modulation of ascending electrosensory information by
TRANSCRIPT
Loyola University Chicago Loyola University Chicago
Loyola eCommons Loyola eCommons
Master's Theses Theses and Dissertations
1994
Modulation of Ascending Electrosensory Information by Modulation of Ascending Electrosensory Information by
Descending Pathway Stimulation in the Channel Catfish Descending Pathway Stimulation in the Channel Catfish
Lizabeth Scoma Loyola University Chicago
Follow this and additional works at: https://ecommons.luc.edu/luc_theses
Part of the Biology Commons
Recommended Citation Recommended Citation Scoma, Lizabeth, "Modulation of Ascending Electrosensory Information by Descending Pathway Stimulation in the Channel Catfish" (1994). Master's Theses. 4064. https://ecommons.luc.edu/luc_theses/4064
This Thesis is brought to you for free and open access by the Theses and Dissertations at Loyola eCommons. It has been accepted for inclusion in Master's Theses by an authorized administrator of Loyola eCommons. For more information, please contact [email protected].
This work is licensed under a Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 License. Copyright © 1994 Lizabeth Scoma
LOYOLA UNIVERSITY CHICAGO
MODULATION OF ASCENDING ELECTROSENSORY INFORMATION
BY DESCENDING PATHWAY STIMULATION IN THE
CHANNEL CATFISH
A THESIS SUBMITTED TO
THE FACULTY OF THE GRADUATE SCHOOL
IN CANDIDACY FOR THE DEGREE OF
MASTER OF SCIENCE
DEPARTMENT OF BIOLOGY
BY
LIZABETH SCOMA
CHICAGO, ILLINOIS
MAY 1994
ACKNOWLEDGEMENTS
I would like to thank my advisor Dr. John G. New for
introducing me to the world of neuroscience. His support and
guidance were invaluable. I would also like to thank my other
committee members, Ors. John Janssen and Richard Fay for their
statistical, scientific and creative assistance. Special
thanks go to Christopher Call, Susan Guggenheim and John Quinn
for technical support. Finally, my deepest gratitude goes to
my parents and two sisters, Amy and Nicole for their unending
moral support.
iii
TABLE OF CONTENTS
ACKNOWLEDGEMENTS
LIST OF FIGURES
LIST OF TABLES
iii
·. . vi
vii
. . viii LIST OF ABBREVIATIONS.
Chapter
I.
II.
III.
IV.
INTRODUCTION 1
Catfish Electrosensory System ...... 5 Electrosensory Processing in the Central
Nervous System . . . . . . . . 8
MATERIALS AND METHODS .. . . 12
Experimental Animals ........... 12 surgical Procedures ........... 12 Electrode Placement . . . . . . ... 13 Constant Stimulus Parameters ..... 13 Inhibition Experiments .......... 14 Voltage Curve Experiments ...... 14 Latency Experiments ........... 14 Frequency Experiments ...... 14 Marking of Recording Site ..... 15 Retrieval of Recording Marks. . ... 15 Data Analysis .............. 16 Analysis Within a Data Block . . . . . 16
RESULTS . . . . . 18
Recovery of Marked Recording Sites .... 18 The Shape of Evoked Potential Waveforms . 18 Effect of Delivering a Electric Pulse
Train to nPr Prior to Electric Field Presentation ............. 19
Results of Varied Amplitude of Electric Pulse Train Delivered to nPr ..... 20
Results of Varied Frequency of Electric Pulse Train Delivered to nPr ..... 21
Duration of nPr's Inhibitory Response .• 22
DISCUSSION • • 36
REFERENCES • . . . . . . . . . . . . . • . • . . . . . • 4 3
iv
LIST OF FIGURES
Figure
1. Circuit Diagram of the Afferent and Efferent Projections of the Electrosensory and Mechanosensory Systems of the Catfish
2. Diagram of stimulus/Recording Paradigm ..
3. An Evoked Potential Waveform Response to Electric Field Presentation Alone and Preceded by nPr Stimulation ...•.
4. A Diagram Illustrating the Amplitude of an nPr Stimulus Train Necessary to Cause Saturated
Page
. 24
. . 25
. 26
Inhibition . . . . . . . . . . ..•.. 27
5. A Diagram Illustrating the Effect of the Frequency of an nPr Stimulus Pulse Train on the Amount of Inhibition Elicited •.••.•• 28
6. A Diagram Illustrating the Duration of nPr's Inhibitory Response •.....••••... 29
vi
LIST OF TABLES
Table Page
1. Results Showing Stimulation of nPr Preceding Electric Field Presentation Inhibits Ascending Electrosensory Information ...•...•... 30
2. Results Showing an Amplitude Threshold Exists for the Activation of nPr. . . . . . . . .•.. 31
3. Results Showing Frequency is Sufficient to Cause nPr Activation . . . . . . ....••••• 32
4. Results Showing nPr's Inhibitory Response is Longer than l00ms in Duration .....•.• 33
5. Results from a Tukey's Multiple Comparison Statistical Analysis on Long Delay Data ..••. 34
6. Results Showing nPr's Inhibitory Response Lasts Between 120 and 480ms ..........• 35
vii
AENs
ALLN
cc
CON
DGR
DON
e
ELLL
EGa
EGp
LLN
m
MON
nPrd
nPrv
PLLN
SEM
TSl
TSm
LIST OF ABBREVIATIONS
afferent electrosensory neurons
anterior lateral line nerve
cerebellar crest
caudal octavolateralis nucleus
dorsal granular ridge
dorsal octavolateralis nucleus
electrosensory
electrosensory lateral line lobe
eminentia granularis anterior
eminentia granularis posterior
lateral line nerve
mechanosensory
medial octavolateralis nucleus
dorsal nucleus praeeminentialis
ventral nucleus praeeminentialis
posterior lateral line nerve
standard error of the mean
lateral torus semicircularis
medial torus semicircularis
viii
CHAPTER I
INTRODUCTION
Central mechanisms of sensory processing in the
vertebrate brain have been the focus of much research, however
relatively little is known about the strategies by which
sensory systems detect and interpret the world. The purpose of
this study is to explore neural strategies using the
electrosensory system of the catfish, Ictalurus punctatus, as
a model, specifically the influence of descending control from
midbrain centers on electrosensory information ascending from
the Medulla.
Electrosensory systems are used to detect and orient to
weak electric fields in the environment. Bioelectric fields
are generated as a result of neural and muscular activity of
both vertebrates and invertebrates, as well as from the
cellular activity of some higher plants. Electric fields can
also be generated by physicochemical sources in the
environment (Roth 1972, Peters & Meek 1973). Electroreceptive
animals use this sense in detecting and orienting toward prey,
locating predators, in some cases communicating with
conspecifics, and possibly in navigation (Kalmijn 1974, Peters
& Bretschneider 1972). One of the earliest descriptions of
electroreception was the demonstration in catfish of behaviors
associated with changes in the earth's magnetic field caused
2
by seismic events (Hatai & Abe 1932, Hatai et al 1932, Kokubo
1934).
Electroreception appears in a number of anamniotic
vertebrate taxa, as well as in two mammalian species; the
duck-billed platypus and the star-nosed mole (Bullock et al
1982, 1983, Scheich et al 1986, Gregory et al 1987, Gould et
al 1993) . There are two phylogenetic categories of
electroreception; primitive and derived. The primitive
electrosensory system is characterized by electroreceptor
organs, called the ampullary organs, that respond to low
frequency (0.2-20Hz) outward current flow (cathodal
stimulation) (Bullock et al 1982, 1983). The primitive system
is so termed because phylogenetic studies of the distribution
of electroreception indicate that such a system was present in
the common ancestor of all vertebrate taxes (Bullock et al
1982, 1983). This primitive electrosensory system is
characterized by the presence of nucleus dorsalis,
electrosensory afference transmitted via the anterior lateral
line nerve exclusively and the negative (cathodal) polarity
preference of the ampullary receptors.
The majority of non-teleost fish and some amphibians
possess the primitive electrosense. Among the agnathans the
Petromyzoniformes (lampreys) are electroreceptive, however the
Myxiniformes (hagfish) lack electroreception. Of the
gnathostomes, all of the chondricthyan fishes, the
Elasmobranchii (sharks, skates and rays) and the Holocephali
3
(chimeras) are electroreceptive. The Crossopterygii (which
includes one (extant) species, the coelacanth), the Dipneusti
(lungfish), and the Polypteriformes are all electroreceptive
groups. Additionally, some urodele and apodan amphibians are
electroreceptive during the aquatic larval stages of their
development (Bullock et al 1982, 1983). Among the primitive
Actinopterygii (ray-finned fishes), the Chondrostei
(paddlefish and sturgeon) are electroreceptive. The immediate
predecessors of the Teleosteii (bony fishes), the Holostei
(gars and bowfins) which have evolved from the Chondrostei,
and most orders of the Teleosteii lack electroreception. This
suggests that the common ancestor of the teleosts probably was
not electroreceptive. These animals lack electroreceptors or
any central nuclei associated with electrosensory processing
(Bullock et al 1982, 1983).
The derived form of electroreception has been re-evolved
independently at least twice and possibly three or four times
in teleost fishes (Greenwood et al 1966, Bullock 1974). Many
of these electroreceptive teleosts live in silty, low light
environments which are not conducive to the use of a visual
system. Electroreception may thus have re-evolved as a
strategy to compensate for this lack of visual cues and to
provide essential information about their environment. Derived
teleost electrosensory systems most likely re-evolved as a
specialization of the mechanosensory lateral line (Figure 1).
The ampullary receptors in this re-evolved system respond to
4
positive (anodal) stimulation.
The derived electrosensory system is much more limited in
its distribution than the primitive electrosense. Re-evolved
electrosenses are found in the Siluriformes (catfish), the
related Gymnotiformes (South American weakly electric fish),
and the Mormyriformes (African weakly electric fish) (Bullock
et al 1982, 1983, Heiligenberg 1986). Except for the
Siluriformes (catfish) and the Xenomystinae (a subfamily of
electric African fishes) the above fish also possess an
electric organ which generates high frequency electric fields
used in locating prey and communicating with conspecifics. The
taxa which possess electric organs also possess two types of
electroreceptors; ampullary and tuberous. The ampullary
receptors respond to external low frequency electrical stimuli
(0.2-20Hz), inward current flow (anodal stimulation) whereas
tuberous receptors respond to the high frequency electric
organ discharges (up to several thousand hertz) (Heiligenberg
1990). Thus catfish represent an intermediate step of
octavolateralis organization between most teleosts which
possess only a mechanosensory lateral line, and gymnotiforms
and mormyriforms, which possess a lateral line, ampullary and
tuberous electroreceptors.
5
Catfish Electrosensory system
The receptor cells of the ampullary organs in catfish
are innervated by fibers of the anterior, middle; and
posterior lateral line nerves. The primary afferent fibers of
the lateral line nerves terminate in a series of medullary and
cerebellar nuclei: the electrosensory lateral line lobe (ELLL) ,
the medial octavolateralis nucleus(MON), the caudal
octavolateralis nucleus (CON), and the eminentia granularis (Eg)
(Figure 1) (Finger 1986). The MON and probably the CON,
receive mechanosensory input whereas the electrosensory
lateral line lobe receives electrosensory input. Anterior and
posterior subdivisions of the eminentia granularis also
receive mechanoreceptor and electroreceptor afferent fiber
input, respectively (Figure 1) (Tong & Finger 1983, New &
Singh 1993) .
The principal target for primary electroreceptor fibers
is the electrosensory lateral line lobe(ELLL). The primary
afferent fibers of the lateral line nerves terminate within
the core of the ELLL, deep to a layer of crest cells. The
electrosensory lobe in catfish can be divided into four
layers. From superficial to deep, these are the molecular
layer (also known as the cerebellar crest), crest cell layer,
intermediate layer of fibers and cells, and a layer of round
cells (Finger 1986).
The parallel, unmyelinated fibers in the superficial
portion of the molecular layer originate from cells of the
6
posterior eminentia granular is. The deeper portion of the
molecular layer contains fibers that originate from the dorsal
portion of the nucleus praeeminentialis (nPrd). This projection
is bilateral, so that a given cell in the nPrd of one side may
project into the molecular layer of the electrosensory lobe of
both sides (Tong & Finger 1983, Finger 1986).
Directly beneath the molecular layer is a layer of large,
multipolar crest cells. The axons of the crest cells comprise
the ascending output neurons for the lemniscal pathway
emerging from the electrosensory lobe. The crest cells possess
elaborate and extensively branched apical dendrites that
extend into the molecular layer and receive synaptic contacts
from the descending parallel fibers. All of these cells have
some basilar dendrites, but some of the crest cells have a
basilar process that extends deep into the intermediate layer
(Mccreery 1977a).
The intermediate layer of the electrosensory lobe is a
complex layer containing a diversity of cell and fiber types.
Within this layer are small granule like neurons, larger
neurons that project to the lobus caudalis, basilar dendrites
of crest cells, and terminals of primary electroreceptor
afferents, as well as terminals from round cells in the
contralateral electrosensory lobe (Finger 1986).
Lastly, the deepest layer of the electrosensory lobe
contains large round bodied cells, the axons of which project
to the intermediate layer of the contralateral electrosensory
7
lobe. Round cells possess dendrites that extend upward into
the lower portion of the intermediate layer.
A lemniscal system is a series of connected nuclei within
the brain that form an ascending system devoted principally to
a single sensory modality and ultimately reach prosencephalic
levels (Nauta & Karten 1970). The ascending electrosensory
pathway within the central nervous system of catfish meets
these criteria. The electrosensory lobe gives rise to an
ascending fiber system, the lateral lemniscus, which ascends
bilaterally through the brain stem and terminates within the
lateral nucleus of the torus semicircularis(TSl). Axon
collaterals from this system also terminate in a metencephalic
nucleus, the nucleus praeeminentialis. This nucleus has
dorsal and ventral portions which receive electrosensory and
mechanosensory input, respectively (see Figure 1). Research
presented in this thesis focuses on the electrosensory dorsal
portion of nucleus praeeminentialis and its effect on
modulating ascending information. The descending parallel
fiber system of the molecular layer of ELLL and MON comprises
both feedback (LLN->ELLL->nPr->ELLL) and feedforward (LLN
>Egl->ELLL) systems regulating the sensory information. The
electrosensory lemniscal system continues from the torus
semicircularis to a diencephalic nucleus, the nucleus
electrosensorius (see Figure 1) (Carr et al 1981, Finger 1986,
Striedter 1991).
8
Electrosensory Processing in the Central Nervous System
Afferent electrosensory fibers in the lateral line nerves
show a high resting discharge rate, approximately 50-100
impulses per second. The primary fiber increases its discharge
frequency in response to inward current (anodal stimulation)
applied to the appropriate receptors. Typical reported changes
in discharge rates are decreases of 50% and increases of 400%
(Roth 1975). The usual "working" range of the fiber may be
much smaller.
The response properties of the neurons in the
electrosensory lobe differ from those of the primary afferents
in three ways: (1) the central neurons are more sensitive than
the primary afferents by approximately one order of magnitude
(2) the central neurons do not exhibit high levels of
spontaneous activity, and (3) different central neurons are
excited by stimuli of differing polarities, whereas receptors
are excited only by anodal stimulation (Andrianov & Ilyinsky
1973, Roth 1975, Mccreery 1977a, for review see Finger 1986).
Two distinctive types of crest cells were described by
Mccreery (1977a). Type I crest cells are excited by cathodal
stimulation and Type II crest cells are excited by anodal
stimulation. Intracellular recordings in these preparations
demonstrate that the type II unit receives monosynaptic
excitatory input from the primary afferent fibers, while the
type I unit receives disynaptic input via an inhibitory
interneuron (Mccreery 1977a).
9
The receptive fields of the two types of crest cells are
distributed randomly across the body surface. The two
functional classes of the crest cells also occur at the same
depth in the electrosensory lobe. Crest cells of both types
appear to be more responsive to lower frequency stimuli than
are primary afferent fibers. The primary afferents respond
maximally to stimuli of approximately 8 Hz, whereas the crest
cells respond maximally at about 3-4 Hz (Mccreery 1977a).
Therefore, the crest cells act as a low frequency bandpass
filter.
The torus semicircularis contains one of the second-order
nuclei of the lemniscal electrosensory pathway in the CNS.
Electrosensory input reaches the lateral portion of the torus
semicircularis(TSl) via the crest cell axons (Knudsen 1977).
On the basis of a number of electrophysiological and
anatomical criteria, Knudsen suggests that the electrosensory
portion of the torus semicircularis is divisible into the two
functional zones: superficial and deep. The input to the
superficial zone is hypothesized to be predominantly from
Mccreery•s type 1 crest cells, while the input to the deep
zone is from McCreery's type 11 crest cells.
In the high frequency sensitive tuberous electrosensory
system of the gymnotiform teleost, Apteronotus leptorhynchus,
Bastian (Bastian & Bratton 1990, Bratton & Bastian 1990) has
found two projections from the nucleus praeeminentialis to the
electrosensory lateral line lobe: one direct, the other
10
indirect. The direct pathway is comprised of neurons from the
nucleus praeeminentialis projecting to the ventral portion of
the molecular layer of the electrosensory lateral line lobe.
It has been suggested that the sensitivity of restricted
populations of output cells in the electrosensory lateral line
lobe are altered by these cells and that they process
temporally and spatially restricted stimuli. They may act to
increase the intensity of the neural representation of
important stimuli (Bratton & Bastian 1990).
The indirect pathway is comprised of multipolar cells of
the nucleus praeeminentialis projecting bilaterally to the
posterior eminentia granular is. Posterior eminentia granular is
efferents project in turn to the electrosensory lateral line
lobe forming its dorsal molecular layer. Hence, these
multipolar cells influence the electrosensory lateral line
lobe through an indirect pathway. It has been hypothesized
that this indirect circuitry may act as a gain control
mechanism operative within the electrosensory lateral line
lobe (Bastian & Bratton 1990).
To summarize, in gymnotiforms the primary afferent
electrosensory neurons terminate on the crest cells of the
electrosensory lobe(ELLL) and the posterior eminentia
granularis. A bilateral projection originating from the ELLL
terminates in the lateral portion of the torus
semicircularis(TSl). Collaterals of this projection terminate
in the nucleus praeeminentialis(nPrd). A projection from the
11
nPrd may in turn descend onto the ELLL forming a feedback
loop(l). In addition, a projection originating from the
nucleus praeeminentialis terminates in the eminentia
granularis which in turn sends a projection down onto the ELLL
forming an indirect feedback loop ( 2) . Al though the direct
pathway is known to exist in catfish, the presence of an
indirect pathway, although likely, has not been experimentally
confirmed.
This study employs the ampullary electrosensory system of
the catfish as a model to examine the role of descending
projections in influencing ascending sensory information in
the vertebrate central nervous system. This system contains
only ampullary receptors and is therefore quite different from
the tuberous system used by Bastian and Bratton 1990. I have
used neurophysiological techniques to examine the influence of
neurons descending from the nucleus praeeminentialis on the
ascending electrosensory information from the electrosensory
lateral line lobe to the torus semicircularis presumably via
direct and indirect pathways.
CHAPTER II
MATERIALS AND METHODS
Experimental Animals
We used 9 Channel catfish, Ictalurus punctatus, for
inhibition experiments, 3 for voltage curves, 2 sets of 5 for
latency and 5 for frequency experiments. These fish were
maintained in aquaria (190-7501) at 22-24°C. Fish were chosen
randomly from 3 tanks. They were approximately 20cm long and
weighed between 50-75g.
Surgical Procedures
Individual specimens were anesthetized with approximately
0.03% tricaine methanesulfonate (MS 222) and placed on a flat
surface with a respiration tube delivering aerated water, inserted
through the mouth. The right medulla, cerebellum and the
contralateral optic tectum were surgically exposed. The fish
was then placed in the experimental tank (25.4 x 43.18cm) mounted
on a vibration isolated table where the animal's head was clamped
in a specially designed holder and the dorsal aspect kept just
above the water surface. The fish was artificially respirated
by a continuous flow of water over the gills. The water
temperature in the tank was approximately 17°C. The fish was
immobilized with a 0.3ml intramuscular injection of O.lM
pancuronium bromide. One hour was allowed before starting the
12
13
experiment to ensure complete recovery from the anesthetic.
Electrode Placement
A glass micropipette recording electrode ( input impedance
less than 1 Megohm) was placed in the electrosensory lateral
line lobe. Accurate placement was confirmed when a uniform
transverse electric field stimulus (150-200uV/cm, 700ms duration)
delivered across the body of the fish elicited an observable
evoked potential response in the electrosensory lateral line
lobe. A stimulating concentric bipolar electrode was placed in
the dorsal nucleus praeeminentialis. Its position was confirmed
when stimulation of the nucleus praeeminentialis elicited an
observable evoked potential in the electrosensory lateral line
lobe. A similar recording electrode was placed in the
contralateral electrosensory torus semicircularis and its position
confirmed by observing evoked potential responses to electric
field stimuli (see Figure 2 for stimulus/recording paradigm).
Constant Stimulus Parameters
Evoked potential waveforms were collected under three
different stimulus paradigms: ( 1) nucleus praeeminentialis
stimulation alone, (2) electric field stimulation alone, and
(3) nucleus praeeminentialis and electric field stimulus combined.
Electric field stimulation was kept steady during all
experimentation at an amplitude of 40volts, duration of 700ms
and field strength between 150-200uv/cm. Only the stimulus
delivered to nucleus praeeminentialis(nPrd) was varied.
14
Inhibition Experiments
The frequency and duration of the stimulus trains del_ivered
to nucleus praeeminentialis were kept constant at lOOHz and 150ms,
respectively. The amplitude of these stimulus trains was set
at 7, 10 and 12volts. Latency, the time difference between the
end of a nucleus praeeminentialis stimulus train and the beginning
of an electric field stimulus, was set at o, 60, and 120ms.
Voltage and latency parameters were tested randomly.
Voltage Curve Experiments
The frequency, latency and train duration of the nucleus
praeeminentialis stimulus trains ~ere kept constant at lOOHz,
Oms and 150ms, respectively. The amplitude of the train stimulus
was varied randomly at o, 2, 4, 5, 7, 10 and 12volts.
Latency Experiments
The amplitude and frequency of the nucleus
praeeminentialis(nPrd) stimulus train were kept constant at
lOvolts and lOOHz, respectively. Latency between the end of the
stimulus train delivered to nPrd and the beginning of the electric
field stimulus was varied randomly at short latencies of O, 20,
40, 60, 80, and lOOms and long latencies of O, 120, 480, 1000,
1500, 2000ms. Controls for each set of experiments were provided
by placing the stimulating electrode on the surface of the brain
above nPrd after the experimental data had been collected and
using Oms latency while stimulating the area.
Frequency Experiments
The amplitude and duration of the stimulus train delivered
15
to nucleus praeeminentialis were kept constant at l0volts and
150ms, respectively. The frequency of the stimulus train was
varied randomly at 10, 20, 40, 83, 166Hz. After recording the
experimental data, the stimulating electrode was place on the
surface of the brain above nPrd and this area was stimulated
at 166Hz to provide a control.
Marking of Recording Site
The recording electrodes were filled with 2M Nacl saturated
with fast green dye. After an experiment was completed the green
dye from the toral recording electrode was iontophoresed at 50u
amps de, pulse interval 15s, pulse duration 2. 9s for approximately
30 minutes. This procedure marked the recording site in the torus
semicircularis.
Retrieval of Recording Marks
After marking the recording site, the fish was decapitated
and its head stored in 4% glutaraldehyde solution for
approximately a week. The brain was then exposed, extracted from
the skull and returned to the 4% glutaraldehyde solution during
two consecutive weeks. The brain was then switched for a week
to a 20% sucrose and 4% glutaraldehyde solution to cryoprotect
the tissue. The meninges of the brain were removed. The brain
was then blocked in a 20% sucrose gelatin solution and stored
for an additional week in 20% sucrose and 4% glutaraldehyde
solution. The tissue was then sectioned into 30um sections on
a freezing microtome, mounted on Chrome-alum subbed slides,
stained in neutral red and coverslipped. The location of the
16
green mark in the torus semicircularis revealed the recording
site.
Data Analysis
Within each experiment there were different stimulus
parameters tested to determine their effect on ascending
electrosensory information. For example, in the inhibition
experiments 7v was tested with o, 60 and 120ms latencies. A data
block would be 7v tested with one latency either 0, 60 or 120ms.
For each data block, 5 averaged waveforms were collected; 2 from
electric field stimulation alone, 2 from nucleus praeeminentialis
and electric field stimulation combined and 1 from nucleus
praeeminentialis alone. These waveforms were the average of 30
sweeps. They were digitized on a Zenith 286 computer with a DAS-
16F A/D conversion board and rectified. A segment from each
waveform which contained the response to electric field onset
was extracted. The segments originated at the electric field
onset and continued in duration for 300 to 350ms. The length
of these segments encompassed entire responses and were kept
constant throughout the calculation of an experiment.
Analysis within a Data Block
A baseline segment, which indicated the horizontal non
response position of waveforms within a data block, was subtracted
from the two segments containing the response to electric field
stimulation alone. This was done to eliminate background artifact.
The segment containing the response to nucleus praeeminenitailis
stimulation alone was subtracted from the two segments containing
17
the response to nucleus praeeminentialis and electric field
stimulus combined. This was done to remove stimulus artifact
and obtain an electric field segment modulated by nucleus
praeeminentialis stimulation (modulated electric field). The
running integrals of the subtracted segments were calculated
using Asystant Plus (Keithley Metrabyte) sofware. The integrals
of the segments containing a electric field response were averaged
and the integrals of the segments containing the modulated
response were averaged. The averaged value of the modulated
response was divided by the averaged value of the electric field
response so as to normalize the experimental to the control.
This normalized number was then multiplied by 100 to obtain what
percentage the modulated response was of the electric field
response. This was done to determine the effect of nucleus
praeeminentialis stimulation on the amplitude of the electric
field response. Each block was calculated and combined to
determine the outcome of each experiment.
CHAPTER III
RESULTS
Recovery of Marked Recording Sites
Of the twenty-seven experiments included in this study,
twenty-six recording sites were marked and out of these, thirteen
were retrieved. All thirteen were recovered from the torus
semicircularis. The recording site retrieval rate was overall
52%.
the Shape of Evoked Potential Waveforms
The evoked potential waveforms varied considerably from
specimen to specimen and between recording sites within the same
animal. The most common waveform recorded from the torus
semicircularis following a DC step electric field presentation
of 150uV/cm oriented with the anode contralateral to the recording
site had an initial positive peak (mean latency of 52.4ms, SEM
8.3) followed by a negative peak (mean latency of 129.9ms, SEM
10.8) again often followed by a positive peak (mean latency
243.lms, SEM 30.8). Another waveform type had an initial positive
peak, negative peak followed by a positive peak at different
mean latencies of 26.5ms, SEM 5.6, 47.lms, SEM 4.7 and 123.5ms,
SEM 1 7, respectively. Other waveforms recorded were a combination
of those described above.
18
19
Effect of Delivering an Electric Pulse Train to nPr Prior to
Electric field Presentation
In these nine experiments, nPr stimulus train duration and
frequency were kept constant at 150mS and l00Hz, respectively.
Nucleus praeeminentialis was stimulated with 7, 10 and 12 volts,
preceding electric field (EF) presentation by o, 60 or 120mS
delays. The electric field strength and duration were maintained
at 150-200uV/cm and 700mS, respectively. In each case there was
inhibition of the response to the electric field recorded from
the contralateral torus semicircularis. A comparison of the
integrals of the averaged waveforms recorded when combining nPr
and electric field stimulation and those recorded following
electric field stimulation alone demonstrated a reduction
reflecting an inhibition of the response to electric fields when
combined with nPr stimulation. Integrals of waveform responses
to electric fields preceded by nPr stimulation (modified electric
fields) were normalized to those of responses to electric field
stimulation alone (unmodified electric fields). Percentages of
modified to unmodified electric field responses were then
calculated (ranged from 69.60% to 87.94%, see Table 1). The
average mean reduction recorded ranged from 12.06% to 30.40%
and the standard error of each mean ranged from 3.43 to 9.76
(see Table 1). A two factor ANOVA was performed with voltage
and delay as main factors with a voltage*delay interaction.
This indicated no significant difference in effect by these
factors on the inhibitory response (volt. p=.556, 71, 2 df; lat.
20
p=.320, 71, 2 df; volt*lat p=.978, 71, 4 df all at alpha=.05).
subsequently the data from the (3x3=) 9 treatment cells were
pooled and a binomial test used to determine if the treatments
affected response (Xf. = 33.8, P < 0.001, df=l). The results showed
significant inhibition. These experiments indicate that there
was inhibition of ascending electric field information when nPr
was stimulated with the above range of parameters.
Results of Varied Amplitude of Electric Pulse Train Delivered
to nPr
Because above results showed no difference between voltages,
a wider range was tested to determine threshold. In three
experiments the frequency and delay of the nPr stimulus train
were kept constant at lOOHz and oms, respectively. The electric
field duration and strength were maintained at 700mS and
approximately 150uV/cm. The voltage of the nPr stimulus train
varied between o, 2, 4, 5, 7, 10 and 12v. The responses exhibited
a threshold at 7v, above which a saturated inhibition of the
response to electric fields occurred. Integrals of waveform
responses to electric fields modified by nPr stimulation were
normalized to those of responses to EF stimulation alone and
converted into percentages. Normalized response integrals ranged
from 106.52% to 57.77%, the average mean reduction recorded ranged
from -6. 52% to 42. 23% and the standard error of each mean ranged
from 1. 05 to 14. 44 (see table 2). A one-way analysis of variance
was calculated for voltage and the results showed a significant
difference within this parameter indicating the possibility of
21
a threshold effect (F=volt. p=.015, 6, 13). Chi-square analysis
revealed that at o, 2, 4, and 5V the amplitude of the response
to an electric field preceded by an nPr stimulus train was not
significantly different from that produced by electric field
stimulation alone (Binomial Test x2 = 1.18, p < .001, df=l).
When the nPr stimulus train amplitude was 7v, 10v or 12v the
response to electric fields preceded by nPr stimulation was
significantly inhibited (Binomial test, exact calculation p=.004).
These data indicate that the amplitude of the nPr train stimulus
had to reach a threshold of approximately 7 vol ts before
inhibiting ascending electric field information. Once threshold
has been reached the level of inhibition remained somewhat
constant (figure 4). This agrees with the previous experiment
in that the amount of inhibition under these conditions is similar
and apparently saturated.
Results of Varied Frequency of Electric Pulse Train Delivered
to nPr
In five separate experiments the amplitude, delay and
duration of the stimulus train delivered to nPr were kept constant
at l0V, oms and 150mS, respectively. The strength and duration
of the electric field stimulus was maintained at 150-200uv/cm
and 700mS, respectively. The frequency of the train stimulus
delivered to nPr was varied between 10, 20, 40, 83, and 166Hz.
The same procedure was followed to obtain the integrals of the
response waveforms for analysis. The results of the subtraction
demonstrated an overall inhibition of electric field response
22
even when presented with one . lmS pulse. The average mean
reduction recorded ranged from 15.09% to 23.645 with 2.0.2% the
only anomaly at 20Hz and the standard error of each mean ranged
from 4. 55 to 12. 85 ( see Table 3) . A one-way analysis of variance
(ANOVA) was performed on the modified electric field response
integrals and showed no significant difference between the amount
of inhibition elicited by the various frequencies (ANOVA p=.352,
19, 4 df). A binomial test was performed on modified electric
field response data and showed a significant inhibition in the
electric field responses preceded by nPr stimulation (X2 = 16. 67,
p < 0.001, df=l). Statistical results indicate that all the
frequencies were inhibitory. The overall inhibitory effect of
the frequencies used is reflected in the plateau shape of figure
5. The only anomaly was 20Hz which appears close to 100% and
therefore to the unmodulated electric field response.
Duration of nPr's Inhibitory Response
In the next set of experiments the amplitude, delay and
duration of the stimulus train delivered to nPr were kept constant
at l0V, oms and 150mS respectively. Five experiments used delays
of o, 20, 40, 60, 80 and l00mS. An additional five experiments
used delays of o, 120, 480, 1000, 1500, and 2000mS. The same
procedure was followed to obtain the integrals of the response
waveforms for analysis. The results of these ten experiments
indicate that the inhibition of an electric field response caused
by nPr stimulation lasted between 120-480mS.
The average mean reduction recorded ranged from 11.18% to
23
35.07% and the standard error of each mean ranged from 6.64 to
12. 48 for the five experiments implementing short latency
durations. The responses to an electric field preceded by nPr
stimulation with delays of O, 40, 60, 80, and lOOmS were not
significantly different from each other as indicated by one way
analysis of variance (lat.p=.536, 5,24df). When compared to a
response to an electric field alone, the electric field preceded
by nPr stimulation was significantly inhibited (Binomial test
X2 = 13.33, p < 0.001, df=l).
The average mean reduction recorded ranged from -1.32% to
46.15% and the standard error of each mean ranged from 1.30 to
8. 71 for the five experiments implementing long latency durations
(see Table 6). A one way analysis of variance was performed on
the latency parameter and the results indicated a significant
difference between them in eliciting responses (lat.p=.001,
5,24df). Using a Tukey's multiple comparison test indicated that
significant differences in latencies were between Oms and 120rns
at an alpha of 0.01 and between 120rns and 480rns at an alpha of
0.05 (see table 5). Using these two different alpha criteria
indicates that nPr's inhibitory response lasts between 120 and
480rns.
24
DESCENDING ASCENDING
I I I I TS■ I TSI I TSI TSm ID • MID BRAIN • ID
I I
nPrd nPrd
• • nPrv nPrv
ID • ---I L I I
EGa,EGp 1
cc EGp IEGa r 1, • • Ill I
' T I
I l 1 f
ELLL MON MON ELLL
• • Ill • ? I C~N
j f I I
CON I I ALLN ID t
1,111
HIND BRAIN 0- PLLN
1,111
Trunk
Figure 1.
Circuit Diagram of the afferent and efferent projections of the electrosensory and mechanosensory systems of the catfish. There are two significant features of this diagram. First, the electrosensory system is virtually parallel to the mechanosensory system in nuclei location and · axonal projections reflecting their common origin. Secondly, That higher brain centers feedback and modulate ascending information.
C\J
c., C1)
a::
Figure 2.
C
E
lJJ
z _J _J
CL
'-
C.
l
c.:, a)
0::
25
Diagram of the stimulus and recording paradigm used in the experiments. A Recording electrode is placed in the medullary electrosensory lateral line lobe (ELLL). Proper placement of the stimulating electrode is confirmed by recording evoked potentials from the ELLL in response to stimulation of nPr. The second recording electrode is placed in the torus semicircularis. Evoked potentials are recorded from the torus to determined the effect of varied stimulus train parameters delivered to nPr.
26
TORAL EVOKED POTENTIAL
A
EF
50 µV L I 00 ms
8
EF
n Pr II I 1H 111111 IHI
Figure 3.
An evoked potential waveform response to electric field presentation alone (A) top is the waveform trace, bottom is a representation of the DC step electric field (200uv/cm) presented and preceded by nPr stimulation (B) top portion of Bis the waveform trace, bottom is a representation of the train stimulus delivered to nPr prior to electric field presentation and the DC step electric field presented (200uv/cm).
120
100
~ 80 0 ~ E-t z 0 60 t)
~ 0
dP 40
20
0
Figure 4.
27
0 2 4 5 7 10 12
VOLTAGE (V)
The data in this graph is from the average of three experiments. All parameters were kept constant (nPr lOOHz, del=Oms & dur=lSOms: EF 40v, dur=700ms & 2oouv/cm). The amplitude of the stimulus train delivered to nPr was varied randomly at 2, 4, 5, 7, 10, and 12v. The evoked potential responses to electric field presentation preceded by nPr stimulation was normalized to the control ( electric field alone). Percentages were calculated and graphed in this figure.
28
120
100
..:i 80 0
~ E-c :z:
60 0 C)
r:.. 0 40
dP
20 1--- EXP -&- CONT 1
0
0 20 40 60 80 100 120 140 160 180
FREQUENCY {Hz}
Figures.
The data in this graph is from the average of five experiments. All parameters were kept constant (nPr l0v, del=0ms & dur=l50ms: EF 40v, dur=700ms & 200uv/cm). The frequency of the stimulus train delivered to nPr was varied randomly at 10, 20, 40, 83, 16GHz. The evoked potential responses to electric field presentation preceded by nPr stimulation was normalized to the control ( electric field alone). Percentages were calculated and graphed in this figure.
29
100
..:I 80 0 c:i:: -E-t z 60 SD EXP 0 CJ --rz..
40 LD EXP
0 -&-
dP SD CONT 20 ~
LD CONT
0
-200 200 600 1000 1400 1800
DELAY (MS)
Figure 6.
The data in this graph is from the average of two sets of five experiments. All parameters were kept constant except for the delay between the offset of the nPr stimulus and the onset of the electric field. In the short delay experiments (SD EXP) the delays varied at o, 20, 40, 60, so, and lOOms (see table 4). In the long delay experiments (LD EXP) the delays varied at O, 120, 480, 1000, 1500, and 2000ms (see table 6). The evoked potential responses to electric field presentation preceded by nPr stimulation was normalized to the control (electric field alone). Percentages were calculated and graphed in this figure.
30
Table 1. Results showing stimulation of nPr preceding electric field presentation inhibits ascending electrosensory information.
VOLT DEL EF+NPR/EF SEM (V} (MS} (%}
7 0 81. 37 4.91
7 60 78.13 9.40
7 120 87.94 5.95
10 0 78.24 9.52
10 60 69.60 6.64
10 120 82.51 3.43
12 0 81.08 7.98
12 60 80.35 9.76
12 120 85.07 5.16
The above table shows the results averaged over nine experiments. Column one and two show the parameters of voltage and delay used when stimulating nPr, respectively. Column three shows what percentage the modified response (electric field preceded by nPr stimulation) is of the control response (electric field alone). The last column shows the standard error of the mean for the percent averages in column three.
31
Table 2. Results showing an amplitude threshold exists for the activation of nPr
VOLTAGE EF+NPR/EF SEM (V) (%)
0 106.52 1.05
2 93.13 11.23
4 94.87 8.64
5 90.72 14.44
7 57.77 1.15
10 69.70 5.11
12 67.50 2.58
The above table shows the results averaged over 3 experiments. The first column indicates the voltages used to stimulate nPr. Column two shows what percentage the modified response (electric field preceded by nPr stimulation) is of the control response (electric field alone) (graphed in figure 4). Column three shows the standard error of the mean for the percent averages in column two.
32
Table 3. Results showing frequency is sufficient to cause nPr activation
FREQUENCY EF+NPR/EF SEM (HZ) (%)
10 76.94 7.81
20 97.98 12.85
40 84.91 5.95
83 84.91 6.29
166 76.36 4.55
166 CONT 98.92 2.72
The above table shows the results averaged over five experiments. The first column indicates the frequency used to stimulate npr. Column two shows what percentage the modified response (electric field preceded by nPr stimulation) is of the control response (electric field alone) (graphed in figure 5). Column three indicates the standard error of the mean for the percent averages in column two.
33
Table 4. Results showing nPr's inhibitory response is longer than l00ms in duration
DELAY EF+NPR/EF SEM (MS) (%)
0 64.93 7.74
20 84.65 12.48
40 74.29 7.60
60 76.63 10.75
80 88.82 9.02
100 81.58 6.64
0 CONT 106.73 7.20
The above table shows the results averaged over five experiments. The first column indicates the time delay between the offset of nPr stimulation and the onset of electric field presentation. Column two shows what percentage the modified response (electric field preceded by nPr stimulation) is of the control response (electric field alone) (graphed in figure 6). Column four shows the standard error of the mean for the percent averages in column two.
34
Table 5. Results from a Tukey' s Multiple Comparison statistical analysis on long delay data
LAT 0 120 480 1000 1500 2000 (MS)
-
RESP 53.85 76.71 97.28 93.89 99.25 101.32 (%)
a=.05 xxxxxx xxxxxx 000000 000000 000000 000000 00000
a=.01 000000 000000 000000 000000 00000
The above table shows the statistical results averaged over five experiments using the Tukey' s multiple comparison analysis. The X's indicate that latencies of o and 120ms are similar in their ability to elicit an inhibitory response. The o's also indicate a statistical similarity in evoking an inhibitory response. The results from using two different alpha values indicate that nPr' s inhibitory response lasts between 120 and 480ms.
35
Table 6. Results showing nPr's inhibitory response lasts between 120 and 480ms
DELAY EF+NPR/EF SEM (MS) (%)
0 53.85 5.90
120 76.71 8.71
480 97.28 2.21
1000 93.89 3.25
1500 99.25 1.30
2000 101.32 2.71
0 CONT 97.62 4.27
The above table shows the results averaged over five experiments. The first column indicates the time delay between the onset of nPr stimulation and electric field presentation. Column two shows what percentage the modified response (electric field preceded by nPr stimulation) is of the control response (electric field alone) (graphed in figure 6). Column four shows the standard error of the mean for the percent averages in column two.
CHAPTER IV
DISCUSSION
We have found that stimulation of nPr causes inhibition
of ascending electrosensory information as recorded from the
torus semicircularis. That this inhibition was strong is shown
by a 14. 93%-30. 40% decrease in response, long lasting ( 120-480mS)
and elicited by just one .lmS pulse. In addition, a stimulus
amplitude threshold of seven volts had be reached before this
inhibition saturated. Descending control from higher brain centers
on lower order nuclei is a recurrent theme in vertebrate neural
strategy. Previous studies in catfish have shown that stimulation
of the cerebellum inhibits the response to electric fields
recorded in the torus semicircularis (Crispino 1983). Crispino
stimulated the superficial region of the cerebellar lobus
caudalis. When he recorded from the electrosensory lateral line
lobe or from the ascending lemniscal fibers leading to the torus
semicircularis following cerebellar stimulation he recorded
no inhibition of the response to electric fields from either
recording site (Crispino 1983). He therefore concluded that he
was stimulating a direct ascending projection from the cerebellar
lobus caudalis to the torus semicircularis. Such a projection
has been anatomically proven to exist and forms a feedback loop
onto the ELLL (Crispino 1983, Tong & Finger 1983) . Why Crispino
36
37
did not see a response in ELLL upon stimulating lobus caudalis
in intact preparations is unclear as it is likely he also
stimulated the descending parallel fiber tracts originating in
Egr and nPr. Perhaps the projection from lobus caudalis to the
ELLL modifies electrosensory information in a more subtle way.
Our work does not dispute this projection but highlights another.
In our experiments, the stimulating electrode was placed deep
within the cerebellum not superficially and location in nPr was
verified by activation of the descending fiber pathway as recorded
in the ELLL. The response recorded in the electrosensory lateral
line lobe was large and resulted only after stimulating in a
localized area in the metencephalon; the nucleus praeeminentialis.
In another study, recording from single units in the ELLL
following nPr stimulation revealed a quick burst of excitatory
activity followed by a pronounced inhibition (New unpublished
data). Other studies have shown the existence of a direct
projection in catfish and gymnotiforms between nPr and ELLL
(Bratton & Bastian 1990, Tong & Finger 1983, Finger & Tong 1984).
An indirect projection between nPr-Egr-ELLL exists in gymnotiforms
and may exist in catfish but has not yet been demonstrated
(Bastian & Bratton 1990). Due to the evoked potential and single
unit responses to nPr stimulation recorded in the electrosensory
lateral line lobe and the demonstrated anatomy in both catfish
and gymnotiforms we are confident that in these experiments we
were stimulating one or more descending projections.
In elasmobranchs, the first order nucleus in the
38
electrosensory system, the dorsal octavolateralis nucleus (DON)
and the output afferent electrosensory neurons (AENs) are similar
to the catfish's electrosensory lateral line lobe (ELLL) and
the lemniscal crest cells, respectively (Bastian & Courtright
1991). The dorsal granular ridge in elasmobranchs is similar
to the eminentia granularis in electroreceptive teleosts and
is the sole source of descending parallel fibers to the DON;
there is no additional projection comparable to the nPr of
teleosts (Bass 1982, Bullock et al. 1983). Conley, working with
the skate, Raja erinacea, recorded from the projection AENs of
the DON a brief burst of excitation followed by prolonged
inhibition of approximately 200mS following DGR stimulation
(Conley 1991, Ph.D. Thesis). This is similar to the responses
observed in single unit recordings from the ELLL in the catfish
following nPr stimulation (New, unpublished data). Our work with
evoked potentials recorded from the torus semicircularis showed
a pronounced inhibition of electric field responses (120-480mS)
after nPr stimulation. Electric field presentation during this
period inhibited the electrosensory response. Crispino found
that stimulating the cerebellum inhibited electrosensory
information recorded from the torus semicircularis (Crispino
1983). In gymnotiforms, Maler et al discovered through the use
of electron microscopy that the dorsal molecular layer from the
EGr makes primarily excitatory contact with the output and
interneurons of the ELLL (Maler et al 1981, Mathieson & Maler,
1988). However, Bastian has found that physiologically, this
39
electrosensory circuit has a primarily inhibitory influence on
ELLL output neurons (Bastian, 1986a, b). When EGr was lesioned
the excitability of the output neurons of ELLL increased as if
inhibition had been removed (Bastian, 1986a, b). Having both
excitation and inhibition in a circuit is advantageous to the
shaping of ascending information.
The results of these studies suggest that descending pathways
to the medullary electrosensory nuclei form the neural substrate
of a "gain control" mechanism. Proper functioning of this
mechanism requires that the amount of ascending information be
quantified and the level modified through descending control
onto the output neurons of the ELLL to obtain the amount of
ascending information necessary for optimal functioning. The
direct and indirect feedback loops in gynotiforms and probably
in siluriforms ELLL-nPr-ELLL and ELLL-nPr-EG-ELLL has nPr
advantageously placed for the quantifying of ascending information
(Bastian & Bratton 1990, Bratton & Bastian 1990). In addition,
Bastian's work has demonstrated that nPr multipolar cells modify
their stable firing rate within about 1 sec of an EOD amplitude
change which illustrates a quickly adapting system (Bastian &
Bratton 1990). The high sensitivity of nPr encoding was
demonstrated by the average spike frequency change of 2 and 3
spikes/sec given an EOD amplitude change of 1% (Bastian & Bratton
1990). Anatomical placement, quick adaptation and high sensitivity
make nPr a strong candidate for quantifying ascending information
and modifying it's ascent through descending projections onto
40
lower order nuclei in gymnotiforms and electrosensory teleosts.
Elasmobranchs do not have a related structure to nPr. However,
electrosensory information descends from the lateral mesencephalic
nucleus to the paralemniscal nucleus to the DON and DGR indicating
descending modification of ascending electrosensory information
(Conley 1991, Ph.D. Thesis).
The purpose of the electrosensory circuits may also be
understood in the context of the searchlight hypothesis,which
suggests a mechanism providing an attentional searchlight in
the brain (Treisman 1977, Treisman & Gelade 1980, Treisman &
Schmidt 1982, Treisman 1983, Crick 1990). The searchlight provides
a neural mechanism by which to monitor activity, determine where
the excitation is, intensify it, turn it off and to finally move
on to the next area of attention. Nucleus praeeminentialis which
receives ascending axon collaterals from ELLL may monitor the
activity in this manner and intensify the excitation via
modulation of descending inhibition. Crick proposed a way in
which a nucleus using the inhibitory neurotransmitter GABA, which
is present in the nPr of catfish and in the lateral line of
goldfish, could produce excitation in a lower nucleus using
positive feedback (Crick 1990, New & Yu 1994). Assume that a
portion of nPr was excited above background via ascending
lemniscal axons. Descending GABAergic projections from nPr will
project locally onto target crest cells in the ELLL and
hyperpolarize them via GABAergic synapses (Llinas & Jahnsen 1982,
Jahnsen & Llinas 1984a; 1984b) . If there is a topographic
41
organization of ascending lemniscal axons and descending nPr
projections, selective activation of populations of crest cells
would result in localized hyperpolarization of these same cells.
Such topographic organization has been demonstrated to exist
in elasmobranchs between DGR and DON (Bodznick & Schmidt 1984,
Schmidt & Bodznick 1987) . Additionally, in thalamic slices from
the guinea pig it has been demonstrated that inhibitory inputs
causing hyperpolarization sensitized these neurons so that when
current was injected a quick excitatory burst was produced
followed by pronounced inhibition (Llinas & Jahnsen 1982, Jahnsen
& Llinas 1984a;1984b). Ascending information from the lateral
line nerves feeds onto the sensitized crest cells of the ELLL
causing a brief burst of excitatory activity followed by a
pronounced inhibition. This is an example of positive feedback
because the excitation is amplified by excitation and the surround
dampened. Once the excitation is isolated it becomes important
to defuse the positive feedback loop so that the attentional
searchlight can focus on a different area giving it mobility.
This can occur via the inhibition following the quick burst of
excitation necessary for the searchlight to attend. Working with
guinea pig, the pronounced inhibition recorded after the burst
of excitatory activity in the thalamic neurons was 80-lS0mS in
duration (Llinas & Jahnsen 1982, Jahnsen & Llinas 1984a; 1984b).
In channel catfish, New has recorded a quick burst of excitatory
activity followed by pronounced inhibition in crest cells of
the ELLL after delivering current to nPr (New unpublished data).
42
In addition, our evoked potential study recorded inhibited
electric field responses from the torus semicircularis following
nPr stimulation which lasted between 120 and 480mS. This
inhibition may allow the positive feedback loop to be defused
and the attentional searchlight to disengage and focus on new
excitatory activity.
REFERENCES
Andrianov G, Ilyinsky o (1973) Some functional properties of central neurons connected with the lateral line organs of the catfish, Ictalurus punctatus. J Comp Physiol 86:365-376
Bass AH (1982) Evolution of the vestibulolateral lobe of the cerebellum in electrorecptive and non-electroreceptive teleosts. J Morph 164:335-348
Bastian J (1986A) Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. J Neurosci 6:553-562
Bastian J (1986B) Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe. J Comp Physiol 158:505-515
Bastian J, Bratton B (1990) Descending control of electroreception.1.properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe. J Neuro 10(4):1226-1240
Bastian J, Courtright J (1991) Morphological correlates of pyramidal cell adaptation rate in electrosensory lateral line lobe of weakly electric fish. J Comp Physiol 158A:393-407
Bodznick D, Schmidt AW (1984) Somatotopy within the medullary electrosensory nucleus of the little skate, Raja erinacea. J Comp Neurol 225:581-590
Bratton B, Bastian J (1990) Descending control of electroreception.11.properties of nucleus praeeminentialis neurons projecting directly to the electrosensory lateral line lobe. J Neuro 10(4):1241-1253
Bullock TH (1974) An essay on the discovery of sensory receptors with an introduction to electroreceptors. In: Fessard A (ed) Handbook of sensoryphysiology. Berlin, Springer-Verlag, Vol III/3 pp 1-12
43
44
Bullock TH (1982) Electroreception. Ann Rev Neurosci 5:121-170
Bullock TH, Bodznick DA, Northcutt RG (1983) The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive sense modality. Brain Res Rev 6:25-46
Carr CE, Maler L, Heiligenberg W, Sas E (1981) Laminar organization of the afferent and efferent systems of the torus semicircularis of gymnotiform fish: morphological substrates for parallel processing in the electrosensory system. J Comp Neurol 203:649-670
Conley RA (1991) Electroreceptive and proprioceptive representations in the dorsal granular ridge of skates: relationship to the dorsal octavolateralis nucleus and electrosensory processing. Ph.D Dissertation, Wesleyan University
Crick F (1984) Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci USA 81:4586-4590
Crispino L (1983) Modification of responses from specific sensory systems in midbrain by cerebellar stimulation: experiments on a teleost fish. J Neuro 49:3-15
Finger TE, Tong SL (1984) Central organization of eighth nerve and mechanosensory lateral line systems in the brainstem of ictalurid catfish. J Comp Neurol 229:129-151
Finger TE (1986) Electroreception in catfish: behavior, anatomy, and electroreception. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp. 287-313
Greenwood PH, Rosen DE, Weitzman SH, Myers GS (1966) Phyletic studies of teleostean fishes, with a provisional classification of living forms. Bull Am Mus Nat Hist 131:339-456
Gould E, Mcshea W, Grand T (1993) Function of the star in Condylura. J Mammalogy 74:108-116
Gregory JE, Iggo A, McIntyre AK, Proske U (1987) Electroreceptors in the platypus. Nature 326:386-387
Hatai s, Abe N (1932) The responses of the catfish. Parasilurus, to earthquakes. Pro Imp Acad Jpn 8:275-378
45
Hatai s, Kokubo s, Abes (1932) The earth currents in relation to the responses of catfish. Proc Imp Acad Jpn 8:478-481
Heiligenberg W (1986) Jamming avoidance responses: Model systems for neuroethology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp. 613-650
Heiligenberg W (1990) Electrosensory systems in fish. Synapse 6:196-206
Jahnsen H, Llinas R (1984) Electrophysiological properties of guinea-pig thalamic neurons-an invitro study. J Physiol 349:205-226
Jahnsen H, Llinas R (1984) Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurons invitro. J Physiol 349:227-247
Kalmiljn AJ (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A (ed) Handbook of sensory physiology. Berlin, Spring-Verlag, Vol III/3 pp.147-200
Knudsen EI (1977) Distinct auditory and lateral line nuclei in the midbrain of catfishes. J Comp Neurol 173:417-432
Kokubo s (1934) on the behavior of catfish in response to galvanic stimuli. Sci Rep Tohuk Univ Biol 9:87-96
Llinas R, Jahnsen H (1982) Electrophysiology of mammalian thalamic neurons invitro. Nature(London) 297:406-408
Maler L, Sas EKB, Rogers J (1981) The cytology of the posterior lateral line lobe of high frequency weakly electric fish(gymnotidae): dendritic differentiation and synnaptic specificity in a simple cortex.
Mathieson WB, Maler L (1988) Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. J Comp Physiol 163:48-506
McCormick CA (1982) The organization of the octavolateralis area in actinoptergian fishes: a new interpretation. J Morph 171:159-181
Mccreery DB (1977A) Two types of electroreceptive lateral lemniscal neurons of the lateral line lobe of the catfish, Ictalurus nebulosus, connections from the lateral line nerve and steady-state frequency response
46
characteristics. J Comp Physiol 113:317-339
Montgomery JC (1981) Origin of the parallel fibers in the cerebellar crest overlying the intermediate nucleus of the elasmobranch hindbrain. J Comp Neural 202:185-191
Nauta WJH, Karten HJ (1970) A general profile of the vertebrate brain with sidelights on the ancestry of cerebral cortex. In: Schmitt FO (ed) The neurosciences: second study program. Rockerfeller Univ Press, New York, pp. 7-26
New JG, Fay C (1994) Distribution of gamma-aminobutyric acid immunoreactivity in the brain of the channel catfish with special reference to octavolateralis systems. Neuroscience Abstract #68.7
New JG, Singh S (1993) Central topography of anterior lateral line nerve projections in the channel catfish, Ictalurus punctatus. Brain Behav Evol 43:34-50
Peters RC, Bretschneider F (1972) Electric phenomena in the habitat of the catfish, Ictalurus nebulosus Les. J Comp Physiol 81:345-363
Peters RC, Meeks F (1973) Catfish and electric fields. Experientia(basel) 29:299-300
Roth A (1972) The function of electroreceptors in catfish. J Comp Physiol 79:113-135
Roth A (1975) Electroreception in catfish: temporal and spatial integration in receptors and central neurons. Exp Brain Res 23(5):179
Scheich H, Langner G, Tidemann c, Coles RB, Guppy A (1986) Electroreception and electrolocation in platypus. Nature 319:401-402
Schmidt AW, Bodznick D (1987) Afferent and efferent connections of the vestibulolateral cerebellum of the little skate, Raja erinacea. Brain Behav Evol 30:282-302
Striedter GF (1991) Auditory, electrosensory, and mechanosenosory lateral line pathways through the forebrain in channel catfish. J Comp Neural 312:311-331
Tong SL, Finger TE (1983) Central organization of the electrosensory lateral line systam in bullhead catfish, Ictalurus nebulosus. J Comp Neur 217:1-16
Treisman A (1977) Focused attention in perception and retrieval of multidimensionaGl stimuli. Percept Psychophys 22:1-11
47
Treisman AM, Gelade G (1980) A feature integration theory of attention. Cognit Psychol 12:97-136
Treisman A, Schmidt H (1982} Illusory conjuctions in the perception of objects. Cognit Psychol 14:107-141
Treisman A (1983} In: Physical and biological processing of images. Braddick OJ, Sleigh AC (eds) Springer, New York pp.316-325
VITA
The author, Lizabeth Scoma, was born on August 31, 1966,
in Chicago, Illinois. In the fall of 1984, she entered Loyola
University Chicago where she received a B.S. in Biology in May
of 1988. During this time, she did undergraduate research for
Dr. John Smarrelli and Dr. Jan Savitz. In August of 1991, she
entered Loyola University Chicago to pursue the degree of Master
of Science under the direction of Dr. John New. Liz was awarded
a fellowship for the years of 1991-1992 and 1992-1993. Her
research was also supported through a Sigma Xi Grant-in-Aid
awarded in 1991.
48
APPROVAL SHEET
The thesis submitted by Lizabeth Scoma has been read and approved by the following committee:
Dr. John G. New, Director Associate Professor, Biology Loyola University Chicago
Dr. John Janssen Professor, Biology Loyola University Chicago
Dr. Richard Fay Professor, Psychology Loyola University Chicago
The final copies have been examined by the director of the thesis and the signature which appears below verifies the fact that any necessary changes have been incorporated and that the thesis is now given final approval by the Committee with reference to content and form.
The thesis is therefore accepted in partial fulfillment of the requirement for the degree of Master of Science
,/7 / /
/ /.-, ~/\ ( ___ ~ ½-4~ Date i 1
Dirictor's sipnature
I