16. A.A. Sokolova and T. D. Llpinetskaya, "Mieroelectrode studies of the motor area of the cortex of the cerebrum in a nonanesthetized rabbit," Zh. Vyssh.Nerv.Deyat., ~, No. 6, 1085-1063 (1966).

17. A.A. Sokolova and T. D. Lipinetskaya, "Microelectrode studies of the reaction of waking In response to various stimuli," Zh. Vyssh. Nerv. Deyat., 18, No. 2, 303-311 (1968).

18. V.M. Storozhuk, Zh. A. gruchenko, and E. F. Semenyuk, "Aetivity of cortleal neurons in conditioned re- flex inhibition, ~' Fiziol. Zh. SSSR, 12, No, 4, 481-489 (1980).

19. V.M. Storozhuk and E. F° Semenyuk, "Dynamics of neuronal reactions in the process of developing a conditioned defensive reflex to sound," Flziol. Zh. SSSR, 10, No. 4, 339-347 (1978).

20. V.M. Storozhukand A. N. Tal'nov, "Reactions of neurons of the somatic cortex of the cat in the instru- mental reflex of placing a paw on a support," Fiziol. Zh. SSSR, ~ No. 4, 392-401 (1982).

21. G. I . Shulgina, Bioelectrieal Activity of the Brain and the Conditioned Reflex [in Russian], Nauka, Mos- cow (1978).

22. A . I . Shumilina, "The conditioned defensive reaction of a deafferented extremity ," in: Problems of Higher Nervous Activity [in Russian], Moscow (1949), pp. 174-185.

23. A . I . Shumilina, "T he participation of the pyramidal and extrapyramidal system in motor activity of a deafferented extremity ," in: Problems of Higher Nervous Activity [in Russian], Nauka, Moscow (1978), pp. 196-207.

24. F. Morell, Electrical Signs of Sensory Coding, Rockefeller Univ. Press , New York (1967).

R E S P O N S E S OF A U D I T O R Y C O R T E X N E U R O N S

IN U N A N E S T H E T I Z E D C A T S TO B E S T - F R E Q U E N C Y

T O N E S

I. O. V o l k o v and A. V. G a l a z y u k IDC 612.825.264:612.825.55

The character is t ics of extra- and intracellutar responses of neurons in the AI region were studied in experiments with unanesthetized cats. It was established that auditory cortex neu- rons with s imilar best frequencies showed different forms of responses to tones of the cor - responding frequency. About 40% of the auditory cortex neurons generated on responses to tone presentation. On-of f and off responses were found in 27% of the neurons. Cortical neu- rons (27%) in which stimulation or inhibition of impulse discharge persisted throughout tone action were assigned to the tonic type group of cells. Approximately 6% of neurons in the AI region did not respond to a tone. During intracellular recording about 85% of the neurons r e - sponded to the turning on and/or off of a tone by generating an action potential followed by an IPSL In 967o of the cortical neurons studied the IPSPs were a constant component of the intracellular responses to a tone. It is concluded that the inhibition of the impulse activity of the given neurons is of pr imari ly a postsynaptic origin. Neurons showing one or an- other form of response differ from one another in the relative intensity and time charac- te r i s t ics of excitatory and inhibitory processes interacting on their postsynaptic mem- branes. In neurons of the phasic type inhibitory processes are dominant over excitatory, while excitatory processes are predominant in neurons of the tonic type.

IN T R O D U C TION

Only a few of the large number of studies devoted to the functional organization of the auditory cortex have been performed on uuanesthetized animals [3, 10, 14, 16]. It has been shown that under these conditions auditory cortex neurons show more complex and diverse forms of responses to acoustic stimulation corn- pared with those obtained under conditions of profound anesthesia [13, 15]. The papers cited present a quali- tative and quantitative description of various types of neuronal responses to tone presentation. However, the question of the heterogeneity of neurons in the auditory cortex, the explanation of which is important for un- derstanding its functional organization, remains little studied. Also insufficiently investigated is the question

A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. TransLated - from Neirofiziologiya, Vol. 17, No. 4, pp. 500-508, July-August, ]985. Original art icle submitted August 9,

1984.

360 0090-2977/85/1704-0360 $09.50 © 1986 Plenum Publishing Corporation

as to which cor t ica l m e c h a n i s m s a r e involved in producing the types of neuronal r e sponses in the audi tory cor tex . In this e6nnection, the goal of the p re sen t pape r included a study, by means of the ex t r ace l lu l a r r e - cording of potent ia ls , of the qual i ta t ive and quant i ta t ive c h a r a c t e r i s t i c s of the var ious f o r m s of ne~dronal r e - sponses in the AI region to tones and, by the in t r ace l lu l a r r ecord ing of potent ials , to s tudy the synapt ic p r o - c e s s e s in the audi tory cor tex involved in producing var ious types of r e s p o n s e s to audi tory s t imulat ion.

M E T H O D

The invest igat ion was conducted under conditions of an acute exper imen t with 15 adult cats . The p r e p - a r a t o r y pa r t of the expe r imen t was p e r f o r m e d under thiopental anes thes ia (single in t raper i tonea t injection a t 40 m g / k g dose ) . The an ima l s were then immobi l i zed with d - tubocura r ine and put under a r t i f i c ia l r e sp i r a t ion . During the next expe r imen ta l per iod the surg ica l f ields and s i tes of fixation of the animal in the s t e r eo tae t i c appara tus were anes thet ized with 0.5~ novocain. The m i c r o e l e c t r o d e invest igat ions were p e r f o r m e d in the AI region, con t ra l a t e ra l to the s ide of acous t ic s t imulat ion, 8-10 h a f t e r anesthet iz ing the an imals . Tone signals , the filling f requency of which was c h a r a c t e r i s t i c of the neurons invest igated, were used as audi tory s t imulat ion. The per iod of the r i s e and fall of sound-s ignal f ronts compr i sed 5 m s e c . The durat ion of tone bu r s t s could v a r y f rom ]0 m s e c to 3 sec . Sound product ion was provided in a wide range of f requencies {from t .0 to 20.0 kHz) with a se t of sound-emi t t ing devices (0.5 GD-37 and 2GD-36 dynamic loudspeakers ) with the app rop r i a t e f requency c h a r a c t e r i s t i c s . The method for acous t ic st imulatiotl and the de terminat ion of be s t f requencies {BF) were desc r ibed in our prev ious pape r [5]. Glass m i c r o e l e c t r o d e s filled with sodium chloride (4.0 m o l e / l i t e r ) with about ]0-12 M~2 r e s i s t a n c e were used for the ex t r ace l lu l a r record ing of cor t ica l neuron potent ials . I n t r a - ce l lu la r r ecord ings were made using g l a s s mic rop ipe t t e s filled with po tass ium c i t ra te (2.0 m o l e / l i t e r ) . To ensure the m o r e effect ive penetra t ion of the cell m e m b r a n e by the m i c r o e l e c t r o d e and a lso to reduce the e l ec - t rode r e s i s t a n c e ( f rom app rox ima te ly 150 to 60 M~), the m i c r o e l e c t r o d e t ip was sharpened using a diamond a b r a s i v e compound at an angle of about 45 °. The neuron impu l se ac t iv i ty in the AI region was r eco rded in the fo rm of s tandard s ignals on magne t ic tape for subsequent ana lys i s on a m i c r o c o m p u t e r .

RESULTS

The extracellular responses were studied in ]80 neurons in AI region to monaural acoustic stimulation with tones of the best frequency for the ceils investigated. About 85% of the auditory cortex neurons possessed a background impulse activity under the experimental conditions, the frequency of which averaged 4/see.

On the basis of the experimental data obtained and also considering the published descriptions of the types of responses of auditory cortex neurons to tones []2-]4], two major groups of neurons were distinguished with phasic and tonic types of response to a BF tone.

Neurons with the phasic type response were located primarily at a depth of 0.6-].2 mm from the cortical surface and comprised 67% of the cells investigated. The majority of phasic type neurons (40% of the total number ) with a shor t la tent per iod (9-15 r e s e t ) responded to tone onset by genera t ing one, m o r e r a r e l y s e v - e ra l action potent ia ls (AP) (on r e s p o n s e ) , followed by a pa r t i a l o r complete inhibition of background ac t iv i ty (Fig. l a ) . At the end of the inhibition per iod, las t ing throughout the duration o f the tone , la te impulse dis-. cha rges f requent ly appeared , the f requency of which m a r k e d l y exceeded the f requency of neuronal background act ivi ty . Approx imate ly 2]% of the neurons developed a phasic r e s p o n s e to both tone on- and offse t ( o n - o f f r e sponse ) (Fig. lb ) . In this case the on r e s p o n s e was gene ra l ly followed by an inhibition of neuronal impu l se d i scharge , the duration of which app rox i m a t e ly coincided in t ime with the act ion of acous t ic stimulation~ ~ae la tent per iod of the off r e s p o n s e was usua l ly 5-10 m s e c longer than the la tent per iod of the on r e sponse , in cer ta in phasic type neurons {about 6%), an inhibition of background act ivi ty commenced a f t e r toneonse t with- out a p reced ing on response . Tone offset evoked a cessa t ion of inhibition and the genera t ion of one o r s ev e ra l APs (off r e sponse ) (Fig. ]c ) . It was noted that a b r i e f ( f rom 10 to 30 m s e c ) inhibition of the neuronal i m - pulse ac t iv i ty a lso occu r r ed a f t e r an off r e sponse , followed by the r e a p p e a r a n c e of background d i scha rges (Fig. lb and e) .

Neurons cha rac t e r i zed by a tonic type of r e s p o n s e compr i sed about 27~ of the cel ls studied. They were found in va r ious l a y e r s of the cor tex; however , m o s t of them were located a t a depth of 1.2-1.8 mrs . This neuron group included about 15% cei ls that, with r e s p e c t to the c h a r a c t e r of r e sponse to a tone, occupied an in t e rmed ia t e posit ion between cor t ica l neurons with pure ly phasic and tonic types of r e sponses . The r e s p o n s e s of the neurons of this group were complex and consis ted of ea r ly and la te components (Fig. ld) . The f i rs t , phasic component co r responded to the ins tant of tone onset , when a neuron with a shor t latent per iod (8-10 m s e c ) gene ra t ed a s e r i e s of impu l ses consis t ing of four to six APs . The second, tonic component compr i sed

361

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Fig. 1. H i s t o g r a m s of d i f ferent types of neuronal r e s p o n s e s in k I region to b e s t - f r e q u e n c y tones . In a - c ) phas ic type r e sponses : on, off, and off r e s p o n s e s , r e spec t ive ly , d and e) Phas ic - ton ic , f) tonic r e s p o n s e s . T ime in m s e c on a b s c i s s a ; n u m b e r of impulses , n, on ordinate . Stimulation m a r k e r beneath h i s t og rams .

the bulk of the neuronal r esponse , mani fes ted in the fo rm of a s table impulse d i scha rge throughout tone action. Frequent ly a t the outset of the record ing of the neuronal r e sponse the phasic component of the r e sponse was followed by a b r i e f ( f rom ]0 to 40 m s e c ) par t ia l o r comple te inhibition of impulse act ivi ty, the ef fec t iveness of which declined during the repea ted act ivat ion of the invest igated cel ls (Fig. ]e ) .

In a few neurons (about 3~0 ) the r e s p o n s e to a tone consis ted only of a tonic component. The r e sponse of these neurons was cha rac t e r i zed by a r e l a t ive ly s teady f requency of impu l ses a r i s ing during the action of the sound s t imulus (Fig. I f ) . The intensif icat ion of acoust ic s t imulat ion, as well as the combination of two d i f fe r - ent sound s t imul i , was accompanied by an i n c r e a s e in impulse f requency in the r e s p o n s e of tonic type neurons . Thus, Fig. 2 i l l u s t r a t e s the effect of an intensif icat ion of neuronal r e sponse during the monaura l presenta t ion of two tone s t imul i of equal f requency and intensi ty. The subs tant ia l i n c r e a s e in the f requency of neuronal i m - pulse d i scha rge obse rved is apparen t ly due to the summat ion of exc i ta to ry p r o c e s s e s on the postsynapt ic m e m - b r a n e of the inves t iga ted cell .

Also ass igned to the group of tonic type neurons were cel ls (about 9?o ) that responded to the p r e s e n t a - tion of a tone b u r s t with an inhibition of impu l se act ivi ty , at the end of which a substant ia l i n c r e a s e in the f r e - quency of background d i scha rge could be obse rved (Fig . 3a) . These neurons were apparen t ly located in the s a m e p a r t the cor tex as neurons of the phaso- ton ic type, s ince in s o m e expe r imen t s we were able to r e co rd r e s p o n s e s of these ce i l s s imul taneous ly using a s ingle m i c r o e l e c t r o d e (Fig. 3b). Opposing r e s p o n s e s deve l - oped in such neurons during exposure to a tone of about 3 see durat ion: inhibition in some and excitat ion in o the rs .

A compara t i ve l y smal l n u m b e r of audi tory cor tex neurons (about 6~ ) were found that did not respond to the presentat ior~of tone s ignals of any frequency. Some did, however , respond with an i n c r e a s e in background f requency to o the r acous t ic s t imuli such as , for example , the rus t l ing of paper , whistling, etc. , but these r e -

362

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o _ ~ R ~ u ~ m ~ 4 ~ : ' J msec

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Fig. 2 Fig. 3

Fig. 2. Histograms of neuronal responses in AI region during monaural presentation of two tone signals, a and b) Histograms of neuronal response to separate stimulation with tones of best frequency (18 kHz) and identical intensity (45 dB), presented from different emitters, c) during stimultaneous presentation of tone stimuli; d) histograms of cortical neuron responses to presentation of prolonged (300 msec) tone burst, e) during com- bination of two tone signals identical in frequency and different in duration. Remaining designations as in Fig. L

Fig. 3. Histograms of responses of opposite directionality of two neurons in AI region recorded simultaneously with single micro- electrode, a) Tonic inhibition of impulse activity of cortical neu- ron; b) phaso-tonie response of another neuron to action of best- frequency tone. Designations same as in Figs. 1 and 2.

sponses were unstable. The frequency of background discharge in many of these cells increased when the microelectrode was moved in the cortex. But a weakening or complete cessation of the background activity was observed when the electrode was held in one position. These neurons were more often observed in the more superficial (I, II) and deep (VI) cortical layers.

In order to clarify the mechanisms involved in forming the described types of responses of auditory cortex neurons to BC tones, their postsynaptic responses were also studied under conditions of the intracel- lular recording of potentials. For the analysis of these responses a group of neurons was selected (30 cells), in the majori ty of which the level of the membrane potential (MP) during intracellular recording was no less than 40 inV. A phasic type of response to tone stimulation was noted in 28 cells (93~). Thus, high-amplitude (from 20 to 40 mV) APs appeared in 80~0 of the cells in response to tone onset during the EPSP ascending phase. Frequently, the repolarization phase of the f i rs t AP coincided with the instant of appearance of the IPSP, during the development of which the impulse activity of the neuron was blocked (Fig, 4a). Often during the presentation of the acoustic stimulus an incomplete suppression of the impulse discharge was observed in the neurons (Fig. 4b). Offset of the tone signal resulted in the cessation of IPSP development and AP genera- tion. Frequently upon tone offset the neuronal phasic response was replaced by a rapid membrane repolar iza- tion, passing to a positive (up to 1 sec) membrane depolarization; the Iatter was accompanied by a tonic im- pulse discharge of the neuron (Fig. 4c). In most of the cells studied the time course of the IPSP roughly co- incided with the t ime of exposure to the tone signal. The duration of such IPSPs could exceed 300 msee, and an inhibition of the neuronal impulse activity was observed throughout this period (Fig. 4d). Also detected were cortical neurons in which high-amplitude (up to 10 mV) and relat ively short (up to 50 msee) IPSPs ap- peared in response to exposure to a tone of any duration (Fig. 4e).

363

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C

l oomsec

Fig. 4. Intracellular neuronal responses in AI region to tone. a) Inhibition of neuronal impulse activity during IPSP development; b) generation of action potential during development of inhibition caused by prolonged (300 msee) sound stimulation; c) phasic ex- citatory response to stimulus onset, and tonic excitatory response to its offset, d) Dependence of IPSP duration upon time of action of sound stimulation; e) development of br ief IPSP.

In some neurons EPSPs appeared upon tone onset that were terminated by IPSPs without achieving the critical MP for AP generation. These neurons responded stably to tone offset by AP generation with a re la- tively short latent period (9-20 rese t ) (Fig. 5).

In one cell the intracellular responses to tone action differed substantially from those described. During the f irs t minutes of intracellular recording at a relatively high MP level (45-50 mV) the neurons responded with the generation of one or, more often, several APs, followed by br ief (20-40 msec) IPSPs. Following in- hibition throughout tone action a powerful depolarization developed, accompanied by a tonic neuronal discharge (Fig. 6}. As apparent from the figure, cessation of sound stimulation caused membrane repolarization to the initial level and the cessation of the tonic neuronal response.

D I S C U S S I O N

The present investigation shows that neurons in the AI region with similar BCs show different forms of responses to tones of the corresponding frequency, indicating the heterogeneity of neuronal organization in the auditory cortex.

A phasic type of response characterized 67% of the auditory cortex neurons, located pr imari ly in cort i - cal layers III and IV. These neurons responded to tone onset and (or) offset with the generation of one or less often several APs. The phasic neuronal response was followed early during stimulation by a partial or com- plete inhibition of impulse activity, lasting throughout the action of the tone.

During presentation of the tone signal, 27% of neurons responded with a steady increase in frequency or an inhibition of impulse discharge and were assigned to the group of neurons of the tonic type. They were found more often in the deeper cortical layers (IV-VI), pr imari ly in layer V.

364

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Fig. 5. In t r ace l lu la r neuronal r e sponse in AI region to tone offset .

Fig. 6. In t race l lu la r r e s p o n s e s of tonic type to tone a t var ious l eve l s of neuron m e m b r a n e potential (43, 30, and 15 mV, r e s p e c - t ively, for a - c ) .

The neurons of the region invest igated mainta ined the i r c h a r a c t e r i s t i c fo rm of r e sponse to the BC tone quite s tably through m a n y hours of exper imenta t ion . However , when the functional s ta te of the cor tex was i m - pa i red (as a r e su l t of hypoxia, overcool ing, the influence of anes the t i cs ) o r a f t e r change in the p a r a m e t e r s of the acous t ic s ignal {frequency or in tens i ty) , substant ia l r eorgan iza t ions could occur in the c h a r a c t e r of the neuronal r e sponse to the tone.

The obtained r e su l t s indicate the g r e a t p redominance in audi tory cor tex neurons of phasic types of r e - sponses ove r tonic. This is cons is tent with the data of a number of authors []0, 16| studying the charactelcis - t ics of the r e sponses of audi tory cor tex neurons of unanesthet ized cats to the act ion of tones. F u r t h e r m o r e , these r e su l t s a r e in a g r e e m e n t with the fact that as the level of organizat ion of the audi tory a f fe ren t pathway is inc reased , the i n c r e a s e in the d ive r s i ty of f o r m s of neuronal r e s p o n s e s in the corresponding nuclei is a c - companied by a sequential i n c r e a s e in the re la t ive n u m b e r of neurons cha rac t e r i zed by a phasic type of r e - sponse [1, 2, ]6-18] .

According to the data of an invest igat ion of in t r aee l lu l a r r e sponses , 85% of neurons in the AI region r e - sponding to a tone responded with A P genera t ion to the onset of acous t ic s t imulat ion. Frequent ly the descend- ing phase of the f i r s t AP coincided in t ime with the instant of appea rance of an IPSP, i .e. , the phas ic exc i ta to ry r e sponse of the neurons was apparen t ly in te r rup ted by an inhibition a t the s t a r t of i t s development . An [PSP was a constant component of the in t r ace l lu l a r r e s p o n s e to a tone in 96% of the cel ls studied. This a g r e e s with the r e su l t s of an investigation of the pos tsynapt ic r e s p o n s e s of neurons in the At region to a cl ick and the e l ec - t r i ca l s t imulat ion of f ibe r s in the genicu locor t ica l t r a c t [9].

Thus, the obse rved inhibition of neuronal impulse ac t iv i ty a r i s ing in r e s p o n s e to tone s t imulat ion is p r i m a r i l y due to the development of a pos tsynapt ic inhibition in the cor t ica l neurons [4, 6, 7]. However , it should be borne in mind h e r e that inhibition a lso develops with some advance in m o s t neurons in the under ly - ing segmen t s of the audi tory pathway, e spec ia l ly in the tha lamic r e l a y nuclei , and in the given ca se b locks the p a s s a g e of impu l ses to the audi tory cor tex [3, 8, ]1] . It has, however , been establ ished, that the in t r acor f i ca l inhibition developing during the presenta t ion of re la t ive ly prolonged tone bu r s t s (300 m s e c and m o r e ) is not a lways suff icient ly effect ive. Thus, for example , during the development of an individual IPSP s e p a r a t e EPSPs could a r i s e , the ampl i tude of which achieved the c r i t i ca l MP for AP genera t ion . F u r t h e r m o r e , the inhibition of impu l ses evoked by tone action during ex t r aee l l u l a r r eco rd ing was in m a n y cases incomplete . The foregoing fac ts indicate that the excitat ion of a speci f ic port ion of the neurons of the med ia l geniculate body during the action of tone s t imul i is so in tense that i t ensu res the effect ive synapt ic act ivat ion of cor t ica l neurons , o v e r - coming the pos t syaap t ic inhibi tory p r o c e s s e s developing in these neurons . It evidently should a lso be a s sumed ~ t the durat ion of inhibi tory p r o c e s s e s in a substant ia l port ion of tha lamic r e l a y neurons is s h o r t e r than in cor t i ca l neurons .

Of definite i n t e r e s t a r e the in t r ace l lu l a r r e sponses of audi tory cor tex neurons responding s tably with AP genera t ion both to tone onset and offset . About 16~ of the neurons responded to tone onset with the de -

365

velopment of a primary IPSP, while upon tone offset they generated a phasic response in the form of an off response. In some cells, instead of the brief phasic response to tone offset a tonic discharge developed against the background of a powerful and prolonged neuronal depolarization. Insofar as the off response in most c a s e s

appeared at the end of the IPSP descending phase, it could be assumed that it arises passively as a conse- quence of postinhtbitory exaltation [3]. However, the possibility cannot be ruled out that the off response in many cortical neurons is an independent response evoked by the arrival in the cortex of an afferent volley as a result of tone offset. In support of this postulate is the fact that IPSP development ceases abruptly upon sound-stimulus offset with a short latent period close to the latent period of the on response, and a rapid neu- ronal depolarization develops. Furthermore, a rather high stability of the latent period of appearance of the off response is evident.

The results of a study of intracellular neuronal responses of the tonic type showed that the tonic im- pulse discharge is due to an extremely intense neuronal depolarization lasting throughout tone action. The reduction of the MP level of a neuron as a result of its injury with the mieroeleetrode caused a rapid inactiva- tion of excitatory processes. In this case the IPSP amplitude and duration increased for some time. The IPSP latent period was reduced markedly, and at a sufficiently low cellular MP was only several milliseconds longer than the EPSP latent period (Fig. 6). This fact indicates a competitive type of interaction between ex- citatory and inhibitory processes, developing nearly simultaneously on the postsynaptic membrane of cortical neurons.

Thus, neurons showing a particular form of response differed from one another in the character of in- teraction of excitatory and inhibitory processes on their postsynaptic membranes. Thus, in the responses of phasic type neurons inhibitory processes were dominant over excitatory. These neurons were capable of an impulse response only to tone onset and/or offset and were in a state of inhibition throughout the subsequent time during which inhibition occurred. By contrast, excitatory processes were predominant in cortical neu- rons characterized by a tonic type of response. It is also important to note that one or another form of re- sponse was not absolutely invariant for a specific category of auditory cortex neurons. The structure of the response could be altered as a function of the changes in such acoustic signal parameters as frequency and intensity [3, 6, 7, 10, 14].

L I T E R A T U R E C I T E D

1. G.V. Gershuni, "Organization of afferent flow and the process of discrimination of signals of various duration," Zh. Vyssh. Nerv. Deyat., 15, No. 2, 260-273 (1965).

2. E.A. Radionova, Functional Characteristics of Neurons in the Cochlear Nuclei and Auditory Function [in Russian], Leningrad (1976).

3. F, N. Serkov, Electrophysiology of the Higher Segments in the Auditory System [in Russian], Nauk. Dumka, Kiev (1977).

4. F .N . Serkov, "Neuronal and synaptic mechanisms ofcortical inhibition," Neirofiziologtya, 16, No. 3,

394-403 (1984). 5. F .N . Serkov and I. O. Volkov, "Responses of auditory cortex neurons in the cat to action of tones of

various frequency and electrical stimulation of corresponding segments of cochlea," Neirofiziologiya, No. 5, 527-534 (1983).

6. F .N . Serkov and I. O. Volkov, "Intraceliular responses of neurons of primary auditory region of cat cortex to tones of various frequency and electrical stimulation of nerve fibers in spiral ganglion," Neirofiziologiya, 1_66, No. 1, 123-131 (1984).

7. F .N . Serkov and I. O. Volkov, "Character is t ics of poststimulus and lateral inhibition in neurons of the primary auditory region of the cat cortex," Neirofiziologiya, 16, No. 2, 194-201 (1984).

8. F .N . Serkov and V. N. Kazakov, Thalamic Neurophysiology [in Russian], Nauk. Dumka, Kiev (1980). 9. F .N. Serkov and E. Sh. Yanovskii, "Responses of auditory cortex neurons to stimulation of geniculo-

cortical f ibers ," N eirofiziolegiya, _4, No. 3, 227-236 (1972). 10. M. Abeles and M. N. Goldstein, "Functional architecture in cat primary auditory cortex: Columnar

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EFFERENT CONNECTIONS OF THE CAT

CAUDATE NUCLEUS STUDIED BY RETROGRADE

AXONAL TRANSPORT OF HORSERADISH

PEROXIDASE

N. N. O l e s h k o UDC 612.826.-612.822

A well-developed descending efferent system of the caudate nucleus has been revealed by re t rograde axonal t ransport of horseradish peroxidase. It consists of numerous projections into the thalamus. A topical differentiation of the connections between the caudate nucleus and the paleostriatum and substantia nigra was found. It was established that the main source of efferent connections of the caudate nucleus were small and medium-sized neurons. It was demonstrated that the subthalamic nucleus has a special role in the descending efferent sys- tem of the caudate nucleus. In addition to the direct connections into the caudate nucleus i tself the subthalamic nucleus has direct connections with the main output s tructures of the caudate nucleus, the paleostriatum, and the substantia nigra. The concept that the descending and as- cending connections are interlinked in the mammalian central nervous system is supported by the resul ts of this investigation into the caudate nucleus.

IN T R O D U C T I O N

At present it is generally accepted that there a re direct projections of the caudate nucleus only into the paleostriatum (globus pallidus and entopeduneular nucleus) and the substantia uigra [2, 20-22, 26]. In addi- tion, by means of morphological and electrophysiological methods it has been demonstrated that there a re numerous direct afferent pathways to the caudate nucleus from almost all levels of the encephalon {from the cortex of the cerebral hemispheres to the blue spot) [4, 17, 23, 29]. The hypothesis that there is a marked predominance of afferent inputs over efferent inputs into the caudate nucleus in this s t ructure is not in agree- ment with the concept that the fiber systems are interlinked in the mammalian central nervous system [ 101. In this regard there has been much debate on the question of the presence of direct projections of the caudate nucleus into the brain cortex [], 7-9, 14, ]91 and thalamus [5, 6, 20, 30], from which the nucleus receives af- ferent impulses via numerous direct connections [2, 4, 23, 291.

In this study an attempt has been made to determine the organization of the direct efferent projections of the caudate nucleus with the aid of re t rograde axonal t ransport of horseradish peroxidase. Prel iminary data have been published in an ear l ie r communication [151.

M E T H O D S

The experiments were conducted on ]2 cats each 2.5-3.5 kg in weight. A 30~ aqueous solution of horse- radish peroxidase solution (Boehringer 1, Sigma VI, or Reanal) was introduced by microinjection into various

A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 17, No. 4, pp. 509-517, July-August, ]985. Original ar t icle submitted September 7, ]984.

0090-2977/85/'1704- 0367 $ 09.50 © 1986 Plenum Publishing Corporation 367