RESPONSES OF NEURONS IN THE AUDITORY

TO SOUND STIMULI

F. N. Serkov and V. M. Storozhuk

CORTEX

UDC 612.825.55;612.014,42

The evoked potential (E P) and the pulse activity of single auditory cortex neurons were re-

corded simultaneously in response to a click and to a tone for cats under nembutal and nem-

butal-chloralose anesthesia. Both extra- and intracellular taps were employed. The ex-

periments showed that the reaction of auditory cortex neurons in response to a click lasts

from 200 to 300 msec. It consists of pulse discharges from several groups of neurons.

Out of 174 neurons observed 8 responded within 4 to 7 msee after a click (before the EP).

One hundred and nine neurons reacted in the range from 7 to 25 msec which coincided with

the initial electropositivity of the EP; 11 neurons were in the range from 40 to I00 msec

and 4 were between 180 and 270 msee. Such a sequence of involvement of different neuron

groups in the reaction is probably accounted for to a large extent by the time dispersion of

the afferent volley. With an intracellular tap slow alterations of membrane potential were

observed in the form of an EPSP with pulses together with subsequent hyperpolarization

lasting 50 to 70 msec and slowly increasing depolarization that reached a maximum after 170 to 200 msec.

The investigation of electrical reactions from auditory cortex neurons by means of microelectrode taps has been rather intensely carried on during the last few years [I, 3, 11, 12, 13, 15, 17, 19, 23]. How-

ever, most of these investigations have been concerned with the question of the tonotopic organization in the auditory cortex.

The characteristics of the reactions from different neurons, the order of their involvement in response

to stimulation, their location in the cortex layers, and the relationship between neuron reactions and evoked

potential components have not been studied sufficiently [I, ii, 15, 17]o The lack of such information rnakes

it difficult to answer the question about the nature of the processes that take place in the auditory cortex

when an afferent volley arrives. This information is needed to determine the source of the variot~s evoked potential components.

The problem posed in the present investigation was to study the ehracteristics and the order of in-

volvement of various auditory cortex neurons in the reaction of acoustic stimulation, the depth of their posi- tion, and to compare the neurons' reactions with the evoked potential components.

METHOD

An intraperitoneal injection of 40 mg per kg weight of nembutal or a mixture of 15 mg of nembutal and

35 mg of chloralose was given to the cat. After a tracheotomy and draining of the fourth ventricle the cortex

of the auditory region was exposed during the investigation of the distribution of evoked responses. For the

study of individual neuron reactions a limited portion of the cortex at the place where the lead-out electrodes

were located was uncovered. The experiments started 8 to 10 h after the injection of the drags, and usually repeated injections of d-tnbocurarine (1.5 to 3.0 rng) and artificial respiration were applied. Glass micro-

pipettes filled with 3 M KCI and having a resistance of 7 to 20 MgI were used for the microelectrode taps.

The brain at the site where the microelectrode was inserted was held with a Plexiglass plate or was bathed

with 4% agar. Potentials were led out from the cortex surface with a spherical silver electrode.

A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Trans- lated from Neirofiziologiya, Voll I, No. 2, pp. 147-157, September-October, 1969. Original article submit- ted June 26, 1969.

q

0107(} C'on,s'u/tdtlt,'~ []urcutG ~ dici.~iott o / I~/~'nnm Pt~/,[i,~/~ir~z (,'t~r[l~,rut[~m. 227 i[c,~t ]?[/!,b'trcct. \=cw }'t~i'/~_ ! N. }'. ]OO] l . ' I l l riA'/zt,~' r(',~'cx'ccd. 7'hs'<~ ~r~ ' [ ( ' [c c~ln.n~d [Jc rc[~rol/imcd for ~xn) t>usf~u,~c ~ciz,(zt,s'uc~(~r wi t tmut [~crtzt[s,~ion o f t/l(' I)u[~/i,'~itcr. [ COl) j" (~/" //IZ's <Lrtl'cic [s ,,~z<dl~zt, le fF~,r~l t / : g~lJh'~tier f u r $15 .00 .

]

113

Fig . 1. E P s of the a u d i t o r y c o r t e x a t v a r i o u s po in t s on i t s s u r f a c e . The n u m b e r s on the b r a i n d i a g r a m iden t i fy the c y t o a r c h i t e c t o n i e a r e a s [20]. An upward e x c u r s i o n on the o s c i l l o g r a m s of t h i s and s u b s e q u e n t f i g u r e s c o r r e s p o n d s to a nega t ive va lue unde r the ac t ive e l e c t r o d e . The s t i m u l a t i o n o c c u r s at the beg inn ing of the b e a m ' s t r a v e r s e .

E l e c t r i c a l a c t i v i t y at the m i c r o e i e c t r o d e was fed th rough a ca thode f o l l o w e r and a l a r g e e l e c t r o d e b e s i d e it d i r e c t l y to an a m p l i f i e r and then to a type St-18 d u a l - b e a m o s c i l l o s c o p e f o r v i s u a l m o n i t o r i n g and f r a m e - b y - f r a m e photography° P r o l o n g e d p h o t o g r a p h i c r e c o r d i n g was c a r r i e d out on mov ing p h o t o g r a p h i c f i lm by m e a n s of a "Meopta" t ape t r a n s p o r t m e c h a n i s m f r o m the s c r e e n of the d u a l - b e a m o s c i l l o s c o p e tube.

P u l s e s hav ing a d u r a t i o n of 0.5 m s e c w e r e supp l i ed f r o m a type 1~S-1 g e n e r a t o r to a 2-GD sound r a d i a t o r which p r o d u c e d c l i c k s of up to 60 dB in t ens i ty . In a n u m b e r of e x p e r i m e n t s the s a m e p u l s e s at an a m p l i t u d e 5 to 10 t i m e s h i g h e r than the t h r e s h o l d va lue s r e q u i r e d to d e v e l o p the m a x i m u m e v o k e d p o t e n t i a l w e r e fed to a m i n i a t u r e h e a r i n g a id d y n a m i c r e c e i v e r p l a c e d in the e a r . In a s h o r t s e r i e s of e x p e r i m e n t s with the ac t i ve n e u r o n e x p o s e d a p r o g r a m of sounds r e c o r d e d on m a g - n e t i c t ape was p r e s e n t e d to the a n i m a l . T h e r e w e r e s ing le and p a i r e d c l i c k s , s e r i e s of c l i c k s , and a l s o pu re tones f r o m 250 to 4000 Hz in the p r o g r a m .

R E S U L T S

The p o t e n t i a l s evoked in r e s p o n s e to a c l i c k a p p e a r e d o v e r a l a r g e a r e a of the a u d i t o r y c o r t e x . Under ou r e x p e r i m e n t a l cond i t ions ( e m e r g e n c e of the a n i m a l f r o m an a n e s t h e t i z e d s ta te ) the E P s t aken f r o m v a r - ious po in t s of the a u d i t o r y c o r t e x w e r e d i f f e r e n t in shape , d u r a t i o n , and l a t e n t p e r i o d (F ig . 1). The E P s t aken f r o m a m a j o r p a r t of the a u d i t o r y c o r t e x had the usua l p lus - m i n u s c o m b i n a t i o n and a l a t en t p e r i o d of 6 to 12 m s e c . The E P s f r o m s o m e p o r t i o n s had an i n i t i a l e l e c t r o n e g a t i v i t y .

The E1 ) hav ing the h i g h e s t a m p l i t u d e and r e s i s t a n c e to a n e s t h e s i a was r e c o r d e d with the e l e c t r o d e l o c a t e d in the u p p e r c o r n e r of the f r o n t e c t o s y l v i a n su l cus . H o w e v e r , i t was d i f f i cu l t to d e t e r m i n e the depth of the m i c r o e l e c t r o d e t a p s in th i s spot . T h e r e f o r e in s tudy ing the E P and the p u l s e a c t i v i t y of neu rons we s e l e c t e d the p o r t i o n of the a u d i t o r y c o r t e x l o c a t e d s o m e w h a t to the f ron t of the su lcus in the v i c in i t y of the f ron t e c t o s y l v i a n convo lu t ion (point 7 in F ig . 1). The E1 ) a t th i s spo t is s t a b l e , had the t y p i c a l shape of a p r i m a r y r e s p o n s e , r e a c h e s an a m p l i t u d e of 400 to 500 #V, and has a l a t en t p e r i o d of 6 to 7 m s e c . W h e r e a s the E1 ) d u r a t i o n in the a u d i t o r y c o r t e x of an i n t ac t ca t r e a c h e s 200 to 300 m s e c and c o n s i s t s of f ive s u c c e s - s ive s t a g e s [4, 21], in ou r e x p e r i m e n t s unde r the in f luence of a n e s t h e s i a i t is ev iden t tha t i t d id not e x c e e d 40-80 m s e c ; the t w o - c o m p o n e n t shape was l e s s p r o n o u n c e d in the in i t i a l e l e c t r o p o s i t i v i t y and in g e n e r a l t h e r e w e r e no l a t e r c o m p o n e n t s in the r e s p o n s e .

The p o r t i o n of the c o r t e x s e l e c t e d was at the b o u n d a r y of the f i r s t and s e c o n d a u d i t o r y r e g i o n s [2]. I ts n e u r o n s can r e s p o n d to both a c o u s t i c and s o m a t i c s t i m u l a t i o n s [9]. They have an output to m o t o r a p p a r a t u s [22]. The c o n f i g u r a t i o n of the c o r t e x ' s s u r f a c e in th i s p a r t m a d e i t p o s s i b l e to d e t e r m i n e f a i r l y a c c u r a t e l y the p o s i t i o n of the e l e c t r o d e t ip to a depth of 1600 #. At a g r e a t e r depth i t w a s a c c o m p l i s h e d with s u b s t a n - t i a l e r r o r s .

In the e x p e r i m e n t s wi th an e x t r a c e l l u l a r t ap r e l a t i v e l y t h i ck e l e c t r o d e s hav ing a r e s i s t a n c e up to 10 M ~ w e r e e m p l o y e d . They w e r e good t aps fo r the p u l s e a c t i v i t y of neu rons s i t u a t e d f a i r l y f a r f r o m the e l e c - t r o d e . C o n s e q u e n t l y in m o s t c a s e s the p u l s e s had nega t ive p o l a r i t y and t h e i r a m p l i t u d e was not o v e r 1 o r 2 mV. At the s a m e t i m e t h e s e neu rons had m o r e b a c k g r o u n d a c t i v i t y which did not e x c e e d 10 p u l s e s / s e c .

Out of 174 neu rons r e c o r d e d 135 took p a r t in the r e a c t i o n s to a c o u s t i c s t i m u l a t i o n . An a n a l y s i s of the r e s p o n s e s showed that the neu ron r e a c t i o n of the a u d i t o r y c o r t e x to a c l i c k has the s a m e d u r a t i o n as the EP. Its d u r a t i o n is not, h o w e v e r , due to l eng thy d i s c h a r g e s of one of the neu rons but to a s e q u e n t i a l i n v o l v e m e n t of s e v e r a l neu ron g r o u p s in the r e a c t i o n . The m a j o r i t y of the neu rons t ak ing p a r t in the r e a c t i o n g e n e r a t e d one o r m o r e p u l s e s (F ig . 2). Even when a p u r e tone l a s t i n g 200 m s e c was u s e d i t d id not c a u s e a con t inuous s e r i e s of p u l s e s but r a t h e r s h o r t d i s c h a r g e s [Fig . 5, (4, 5)].

114

F i g . 2. R e a c t i o n s of s e p a r a t e n e u r o n s (upper c u r v e s ) and E P s of the a u d i t o r y c o r t e x ( l ower e u r v e s ) in r e s p o n s e to a c l i c k : (1) and (2) r e s p o n s e s of a s h o r t - l a t e n c y n e u r o n with s low and r a p i d scann ing ; (3) and (4) the s a m e f o r a n o t h e r neuron ; (5) to (12) v a r i o u s r e s p o n s e s of neu rons to a c l i ck . The t i m e m a r k e r s on o s e i t l o g r a m s (2) and (4) a r e 4 m s e e long, and the o t h e r s a r e 20 m s e e .

By eomparing the involvement time of neurons in a reaction with the development time for the EP com-

ponents it is possible to distinguish the following neuron groups. A small group (eight neurons) is involved

in the reaction even before the appearance of the EP. The second, a very numerous group (109 neurons),

reacted during the interval from 7 to 25 msec after the stimulation, i.e., in the initial positive stage of an

El D (Fig. 3). Seven neurons of this group generated a series of pulses in response to a click that started in

the positive stage of the EP and continued during the subsequent negativity. The series consisted of I0 to

15 pulses at a repetition rate as high as 500 per second (Fig. 2, 7).

The neurons of these two groups were characterized by high stability of the responses and uniformity

of the latent period. The histogram of the standard deviations for the latent periods of 87 neurons indicates

that not one of the neurons went over 2.5 msec, and 50 of the neurons were 1 msec or less (Fig. 3, insert).

Erulcar and his collaborators [ii] separated the neurons that reacted during the interval between 5

to 12 msec from those in the interval between 15 and 40 msec after a click, which corresponds to the time of the

appearance of the first and second electropositive EP components for an intact cat. In our experiments,

as may be seen from the histogram of the latent periods (Fig. 3), the first group of neurons shows up well

but the second group is represented by a comparatively small number of neurons, which is evidently con-

nected with the effect of anesthesia and the suppression of the second component of the initial electropositiv-

i t y [41.

The h i s t o g r a m f o r the dep th l o c a t i o n s of n e u r o n s tha t r e a c t d u r i n g the i n i t i a l E P c o m p o n e n t s shows that about half of them are located at a depth between 1200 and 1600 ~ while the rest are in the surface and

the deeper cortex layers, i.e., the neurons of practically all cortex layers are involved in the reaction to

a click. Eleven neurons reacted to a click in the interval between 40 and i00 msee. In three cases these

were discharges of neurons that had generated pulses at the start of the reaetion (Fig. 2, 8-12). The re-

maining eight neurons of this group gave such a late response that it did not react during the initial electro-

positivity. Unlike the stable responses of neurons reacting at the start of the EP development, the late

neuron reactions showed great variability (g -> 5-10 msec). Some neurons of the auditory cortex began to

115

tO 20 30

400

800 i f200

160O

2000 •

I • t • • fS~-m I ~ I

/ 3 • 2 I 3! I 20 t t2 I f* P"-T"n z z

Fig. 3. D i s t r i b u t i o n of n e u r o n s r e a c t i n g to a c l ick d u r i n g the f i r s t 30 m s e c as a func t ion of the l a t en t pe r iod of the r e s p o n s e and of loca t ion depth. The a b s c i s s a shows t i m e in m s e c and the o rd ina t e shows depth in g. The poin ts a re the ave r age l a ten t pe r iods of s e p a r a t e n e u r o n s (5 to 60 r e - sponses ) . Below is a h i s t o g r a m of the n e u r o n s ' d i s t r i b u - t ion as a f unc t i on of the l a t en t r e s p o n s e pe r iods ; at the r igh t is a h i s t o g r a m of t he i r d i s t r i b u t i o n a c c o r d i ng to depth in the cor tex ; the i n se t is a h i s t o g r a m of the s t a n d a r d dev ia t ions for the l a ten t pe r iods of 87 n e u r o n s .

Fig. 4. Late n e u r o n d i s c h a r g e s and E Ps of the audi - t o ry c o r t e x with v a r i o u s s t i m u l a t i o n r a t e s .

r e s p o n d to c l icks a f t e r many r epe t i t i ons . These in i t i a l ly "pass ive" ne u r ons r e a c t e d to c l i cks with pulse d i s c h a r g e s tha t o c c u r r e d f r o m 180 to 270 m s e c a f t e r a c l ick. The r e s p o n s e s c o n s i s t e d of a s e r i e s of pu l se s u sua l l y l a s t i ng about 100 m s e e . They may well follow a f t e r r h y t h m i c s t i m u l a t i o n s (Fig. 4, 2). If, a f t e r a "pas s ive" n e u r o n has b e e n conve r t ed into an "ac t ive" one, a p a i r e d o r s e r i a l s t i m u l a t i o n is appl ied ove r i n t e r v a l s somewha t l e s s than the l a t en t r e s p o n s e pe r iod of such a ne u r on , c o i n c i d e n c e s may be s e e n be - tween the n e u r o n r e s p o n s e s and the e l e c t r o p o s i t i v i t y of the s u b s e q u e n t E P s (Fig. 4, 3-5) . Ev iden t ly , for s o m e n e u r o n s a c l i ck a f t e r 180 to 270 m s e c l eads to i n c r e a s e d exc i t ab i l i ty . Th i s m a y cause a la te d i s - cha rge to o c c u r or , if a s econd c l i ck ac t s in th i s t i m e , to the usua l s h o r t - l a t e n c y d i s c h a r g e .

116

Fig. 5. Reac t i ons of an aud i to ry co r t ex neu - r on with an i n t r a c e l l u l a r tap: (1) for r h y t h m i c s t i m u l a t i o n with a 75 m s e c i n t e r v a l be tween c l i cks (on the r igh t is a r e s p o n s e to p a i r e d s t i m u l i having an i n t e r v a l of 100 msee ) ; (2) and (3) the s a m e with 155 and 220 m s e e in - t e r v a l s be tween s t i m u l i ; (4) r e a c t i o n of the s a m e neu ron when a 250 Hz tone was swi tch- ed on; (5) the s a m e when the tone was 500 Hz. In addi t ion to the E P s the lower beam r e c o r d e d the c l i ck and tones suppl ied.

F o r a por t ion of the n e u r o n s the po ten t i a l s were tapped i n t r a e e i i u l a r l y . F i n e r e l e c t r o d e s having a r e - s i s t a n c e of about 20 M a w e r e used in th i s case . When punc tu red , m o s t of the n e u r o n s g e n e r a t e d d i s c h a r g e s at high r a t e due to the i n j u r y and were de s t royed . On ind iv idua l neu rons the pu lse r a t e was r educed g r a d u a l - ly a f t e r the i n j u r y to 10 pe r second or l e s s . A c l ick evoked a s m a l l E P S P on which the re developed one o r m o r e peak po ten t i a l s of up to 50 mV ampl i tude (Fig. 5). Fo l lowing a d i s c h a r g e was a welt deve loped h y p e r p o l a r - i za t ion of 50 to 70 m s e c d u r a t i o n and an ampl i tude of about 10 mV. Af te r h y p e r p o l a r i z a t i o n the re was s o m e - t i m e s a g r adua l ly i n c r e a s i n g s u b s e q u e n t d e p o l a r i z a t i o n that r eached a m a x i m u m in 80 to 200 m s e c (Fig. 5, 3). F o r r h y t h m i c s t i m u l a t i o n hav ing an i n t e r v a l of 75 m s e c be tween c l i cks only an E P S P without pu l se g e n e r a t i o n takes p lace in r e s p o n s e to some cl icks° The s a m e thing was o b s e r v e d when p a i r e d c l i cks having a s m a l l i n t e r v a l be tween them were used (Fig. 5, 1). When the i n t e r v a l be tween c l i cks was i n c r e a s e d to 150 rosen, the n e u r o n r e a c t e d to e v e r y c l i ek but the r e s p o n s e often c ons i s t e d of j u s t a s ing le pu l se (Fig. 5, 2). Only when the i n t e r v a l be tween s t i m u l i was i n c r e a s e d to 220 m s e c was a f u l l - v a l u e d r e s p o n s e developed by e v e r y c l ick (Fig. 5 ,3) .

In some e x p e r i m e n t s we r e c o r d e d the po ten t i a l s of aud i to ry c o r t e x n e u r o n s for both a c l i ck and for pure tones . Since the po r t i on of the aud i to ry co r t ex inves t iga t ed takes in the s e n s i t i v i t y zone for low tones [15], we employed tones having a f r e que nc y of 250 and 500 Hz. The tone d u r a t i o n was 200 rosen. F igu re 5 shows r e s p o n s e s of one and the s a m e n e u r o n for c l i cks and tones with an i n t r a c e l t u l a r tap. In r e - sponse to the connec t ion of one tone o r the o the r t he re was the s a m e e l e c t r i c a l r e a c t i o n as for a

click: at first an EPSP and then one or more peak potentials, after which hyperpolarization develop- ed.

Subsequently the reaction with tones of 250 and 500 Hz frequency took place somewhat peculiarly. Un-

der the influence of the 500 Hz tone the hyperpolarization shifted slowly with increasing depolarization having

in the background an EPSP with a batch of peak potentials that ceased when hyperpolarization appeared (Fig.

5, 5). Cutting off the tone led to either an EIDSP alone or an EPSP with a peak potential. When a 250 Hz

tone was acting, there was normally only an EPSP without peak potentials. Cutting off the tone either pro- duced no reaction or evoked a small EPSP.

In o r d e r to ob ta in m o r e a c c u r a t e i n f o r m a t i o n about n e u r o n r e a c t i o n s for a s e r i e s of s t i m u l i , a s tudy was made of the pu l se r e s p o n s e s to a s e r i e s of e l i eks (for t0 c l i cks in a s e r i e s ) hav ing i n t e v a l s of 75, 155, 220, and 385 m s e e . The pu l s e s , which were r e c o r d e d for each i n t e r v a l du r ing the r e s p o n s e s of all e ight n e u r o n s , we re s u m m e d and c o m p a r e d with the n u m b e r of pu l se s f r o m these s a m e n e u r o n s in r e s p o n s e s to 10 c l i cks each d e l i v e r e d e v e r y 2 see. It t u r n e d out that when the i n t e r v a l be tween c l i cks was 75 m s e e , the a v e r a g e n u m b e r of p u l s e s in a r e s p o n s e amoun ted to about 21% of the n u m b e r of pu l se s in a r e s p o n s e to c l i cks d e l i v e r e d with a 2 see i n t e rva l . Even with an i n t e r v a l of 385 m s e c the n u m b e r of pu l se s only r a n to 73~0, i . e . , the pu l se r e s p o n s e is r e e s t a b l i s h e d v e r y s lowly, tn th is connec t ion i t is of spec i a l i n t e r e s t to note that for an i n t e r v a I of 220 m s e e , which is n e a r l y the t ime to the i n t e r v a l s for the la te neu ron pu l se r e - ac t ions to a c l i ck and which r e c o r d e d i n t r a c e l l u l a r l y a s lowly i n c r e a s i n g depo la r i za t i on , the n u m b e r of pu l se s in a r e s p o n s e r e a c h e s 84% (Fig. 6, A-E) . It is s e e n f r o m the h i s t o g r a m s for the d i s t r i b u t i o n of pu l ses with r e s p e c t to the t ime of t h e i r i n v o l v e m e n t in the r e a c t i o n that when the i n t e r v a l be tween c l i cks is r educed , the f o r m a t i o n of p u l s e s in the l a t e r s t ages of the r e a c t i o n a re for the m o s t p a r t s topped.

117

20 20

1 10 10

I0 ~tO lO ttO

10 3 ~

tO ~O 10 ~0

7} ,s~ 2~o 3~5

Fig. 6. Tota l p o s t s t i m n l i h i s t o g r a m s of the r e s p o n s e s of e ight neu rons to a s e r i e s of 10 s t i m u l i (c l icks) : A- D) i n t e r v a l s be tween c l i cks 75, 155, 220, and 385 m s e c . Light h i s t o g r a m (A) shows the s a m e for an i n - t e r v a l of 2 sec be tween c l i cks ; E) dependence of n u m - b e r of p u l s e s in a r e s p o n s e on s t i m u l a t i o n f requency . A b s c i s s a - t ime , m s e c ; o rd ina t e - n u m b e r of pu l s e s . E) As a p e r c e n t a g e (the n u m b e r of pu l se s in a 2 sec i n t e r v a l was t aken as 100%). F: 1, 2) n e u r o n r e s p o n s e and EP on c l i ck i n t e ns i t y (60 dB) ; 3, 4) r e s p o n s e on c l i ck t h r e s h o l d in t ens i ty ; 2 and 4 show the s u p e r p o s i - t ion of two r e s p o n s e s .

We obta ined some unexpec ted r e s u l t s when s tudying the r e l a t i o n of the n u m b e r of pu l ses in a r e s p o n s e to the s t r eng th of the s t i m u l a t i o n . The n a t u r e of th is r e l a t i o n s h i p has a l r e a dy been d e t e r m i n e d quite accu- r a t e l y [1] and is suppor ted in the m a i n by the data obta ined. Along with this we were able to obse r ve that a r educ t ion of the s t i m u l a t i o n i n t e n s i t y in the t h r e sho l d r e g i o n was often a c c ompa n i e d by an i n c r e a s e r a t h e r than a d e c r e a s e in the n u m b e r of pu l se s pe r r e s p o n s e . While the p robab i l i t y of o c c u r r e n c e for the s a m e r e s p o n s e was d imin i shed , the l a t en t pe r iod and i ts v a r i a b i l i t y were i n c r e a s e d (Fig. 6, F). It can be con- j e c t u r e d that in a r e s p o n s e for the l oude r c l i cks , not only E P S P s a re p roduced in the ne u r ons of the aud i to ry co r t ex but a lso h y p e r p o l a r i z a t i o n is developed e a r l i e r and m o r e i n t ense ly , thus cut t ing off f u r t h e r pu lse gene ra t i on .

D I S C U S S I O N O F R E S U L T S

In th is m a n n e r the r e a c t i o n of the aud i to ry co r t ex n e u r o n s to an acous t ic c l ick l a s t s for app rox ima te ly 200 to 300 m s e c , which c o r r e s p o n d s roughly to the du ra t i on of the E P in the audi tory co r t ex of an in tac t ca t [4, 21]. The i n v o l v e m e n t of s e v e r a l g roups of neu rons in this r e a c t i o n takes p lace in s t r i c t s u c c e s s i o n d u r i n g spec i f ic t i m e i n t e r v a l s fol lowing the s t imu la t i on . This sequence r e s u l t s f r o m the fact that when s t i m u l a t e d by a c l ick, t he re o c c u r s in the aud i to ry cor tex not j u s t a s ing le shor t vol ley of pu l ses but s e v e r a l s u c c e s - "sive flows which a re f o r m e d as a r e s u l t of the t ime d i s p e r s i o n of an a f fe ren t vo l ley du r ing i t s j ou r ney through the c e r e b r a l cor tex . This can be c o r r o b o r a t e d by the data obta ined in a s tudy of the r e a c t i o n s f r o m sep- a ra t e n e u r o n s of the m e d i a l gen icu la t e body [7]. The i r r e a c t i o n to a c l i ck l a s t ed about 200 mse c . ~n this

118

case th ree groups of neurons a re d is t inguished that r e a c t with la tent pe r iods of 7 to 10, 11 to 25, and 80 to 200 msec a f te r a cl ick. Consequently, the audi tory co r t ex neurons r ece ive an af ferent vol ley with a p r e - d e t e r m i n e d shape that is c r e a t e d dur ing i ts movement to the c e r e b r a l cor tex . This does not e l imina te the poss ib i l i t y of a regrouping ef the pulses in the co r t ex i t se l f during t h e i r t r a n s m i s s i o n f rom one neuron to another . It can be a s sumed that the t ime d i s pe r s i on of an afferent vol ley is addi t ional ly coded so that even when acted on by such a s imple s t imulus as a cl ick, it is not a compact vol ley of pu lses that a r r i v e s at the cor tex , as is the case in the audi tory nerve , but the i r complex aggrega te having a s p a c e - t ime d i s t r ibu t ion which is s t r i c t l y spec i f ied for e v e r y s t imulus and which p rov ides the bas i s of the mechan i sm for d i s t ingu i sh- lag one audi tory s t imulus f rom another°

How this t ime d i s p e r s i o n is brought about and such an aggregate of pu lses is fo rmed is diff icult to ex- p la in at p resen t , tt i s thought that the path f rom the r e c e p t o r s of the cochlea to the neurons of the audi tory co r t ex contains five synapt ic r e l a y s [6, 14]. This might expla in the a r r i v a l of pu l ses at the aud i to ry co r t ex 8 to 10 msec a f te r p re sen t ing a c l ick.

It must be admit ted there exis t , for pulse groups a r r i v i n g at the audi tory co r t ex 15 to 25 msec af te r a s t imula t ion , o ther paths having a lower pas sage ve loc i ty that is , poss ib ly , due to an i n c r e a s e d number of synapt ic r e l a y s . Still more diff icul t to expla in is the appearance in the genicula te bodies of pulse groups 80 to 200 msec a f te r a cl ick. Apparen t ly they develop as the r e s u l t of propagat ion of the exc i ta t ion in the genicula te bodies t hemse lves .

It is a lso diff icul t to expla in the fo rmat ion of a group of pulse r e s p o n s e s in the audi tory cor tex which has a la tent pe r iod of 4 to 6 msec . tf i t is kept in mind that f rom the moment when a sound ac ts on the t ym- panic m e m b r a n e to the appea rance of pu l ses on the audi tory nerve only one msec e l apses [10], then a m e r e 3 to 5 msec r e m a i n s for the r e s t of the t r a n s m i s s i o n which is c l e a r l y insuff ic ient for the pas sage of a pulse over a d i s tance of s e v e r a l c e n t i m e t e r s with five synapt ic r e l a y s . C lea r ly there mus t be in the audi tory s y s - tem, as ide f rom the usual af ferent paths, a path having only two or three synapt ic r e l a y s along which in fo r - mat ion is p a s s e d more rap id ly .

The data f rom our expe r imen t s does not suppor t the widely held concept that the afferent vol ley p r o - duced by a c l ick p a s s e s f i r s t to neurons of the th i rd and fourth co r t i ca l l a ye r s , and only a f te r this does the exc i ta t ion t r a n s f e r to the o ther c o r t i c a l l aye r s . The h i s t og ram for the depth d i s t r ibu t ion of neurons r e a c t - ing during an in te rva l up to 30 msec shows that even in the ve ry beginning of the r eac t ion ali c o r t i c a l l a y e r s a re involved.

By compar ing our data with the r e su l t s f rom a study of neuron reac t ions for the s o m a t o - s e n s o r y c o r - tex in r e sponse to a s ingle nerve s t imula t ion [5] i t is e a s i l y d i s cove red that there is much in gene ra l to in- d ica te the ex i s t ence of common p r inc ip l e s of r eac t ion and informat ion p r o c e s s i n g in these s e ns o r y s y s t e m s . The d i f fe rence is that there a re in the audi tory co r t ex a group of neurons that r espond to an af ferent vol ley with a s e r i e s of h igh- f requency pulses . In addition, the g r e a t m a j o r i t y of r eac t ing neurons (125 out of 137) began to respond during the posi t ive stage of an Et? while in the s o m a t o - s e n s o r y cor tex only two- th i rds of the responding neurons were involved dur ing this s tage.

A comparison of the reactions from the auditory cortex neurons to a click with the EP components in-

dicates that only two components of the initial electropositivity are accompanied by neuron pulse reactions. The initial electronegativity and the later components of the E P, although accompanied by discharges from

a certain number of neurons, are neuron reactions at a level that completely disagrees with the value of the

EP components indicated. As the intervals between clicks is reduced, the neuron pulse reactions to sub-

sequent clicks are cut off for intervals that are relatively longer than those for which the EPs disappear. All this points to the lack of strong correlation between these two forms of electrical activity in the auditory cortex of the brain.

The data we have obtained with intracellular taps showed that a long and complex electrical reaction

is produced in the neurons of the auditory cortex in response to a click. It begins with the usual EPSP on

which are superposed one or more peak potentials, then a pronounced hyperpolarization lasting about 50

msec develops, and after that a still longer, gradually increasing depolarization, so that the total length of the reaction can reach 200 msec. We have not discovered in the literature any data on the reaction of

auditory cortex neurons to a click with intracellular taps. But reactions to a click just like those described

were obtained with intraeellular taps from neurons of the lower tubercles of the corpora quadrigemina. The reaction in these neurons also began with EPSPs in the course of which one or two spike potentials occurred,

followed by the development of prolonged hyperpolarization. It was demonstrated that this hyperpolarization

119

indicated an active inhibition process , i . e . , it is IPSP. Similar hyperpolar izat ion was observed in neurons of other ce rebra l s t ruc tures and is regarded as an indication of r ecur ren t inhibition [8]. It can be assumed that the hyperpolar izat ion we observed in the auditory cor tex neurons also occurs because of the deveIop- ment of r ecu r r en t inhibition.

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

1. G . A . Vardapetyan, "Charac ter i s t ics of react ions f rom neurons of the auditory cor tex of the cat," in: Hearing Mechanisms [in Russian], Nauka (1967), pp.74-90.

2. K. Vulci, "Organization of the auditory cortex," in: Theory of Communication in Sensory Systems [Russian translation], Mir (1964), pp. 251-271.

3. Ya. Katsuki, "Nerve mechanisms of acoustic sensations in the cat ," in: Theory of Communication in Sensory Systems [Russian translation], Mir, Moscow (1964), pp. 288-305.

4. P . M . Serkov and I. I. Shelest, "Evoked potentials in the cerebra l cor tex for acoustic stimulation under the conditions of a t iming experiment ," Fiziol. Zhurn. , AN UkrSSR, 15, 3-10 (1969).

5. V . M . Storozhuk, "Activity of neurons in the f i r s t projection zone of the soma to - senso ry cor tex during a p r imary response ," Zhur. Vussh. Nerbn. Deyat. , 18, 469 (1968).

6. H . W . Ades, "Central auditory mechanisms ," in: Handbook of Physiology, Neurophysiology, Vol. 1 (1959), pp. 581-613.

7. I. M. Aitkin and S. W. Dunlop, "Interplay of excitation and inhibition in the cat medial geniculate body," J. Neurophysiol., 31, 44-62 (1968).

8. P. Andersen, J. C. Eccles, and T. A. Sears, "The ventro-basal complex of the thalamus: types of cells, their responses and their functional organization," J. Physiol., 174, 370-399 (1964).

9. M. Carreras and S. A. Andersson, "Functional properties of neurons of the anterior eetosylvian gyrus of the cat," J. Neurophysiol., 26, 100-126 (1963).

I0. H. Davis, "Excitation of auditory receptors," in: Handbook of Physiology, Neurophysiology, Vol. i (1959), pp. 565-584.

ii. S.D. Erulcar, J. E. Rose, and P. W. Davies, "Single unit activity in the cat," Johns Hopk. Hosp. Bull., 99, 55-86 (1956).

12. E.F. Evans and J. C. Whitfield, "Classification of unit responses in auditory cortex of the unanaes- thetized and unrestrained cat," J. Physiol., 171, 476-493 (1964).

13. E . F . Evans, H. F. Ross, and J. C. Whitfield, "The spatial c lassif icat ion of unit charac te r i s t i c frequency in the p r i m a r y and auditory cor tex of the cat ," J. Phys io l . , 179, 238-247 {1965).

14. R. Galambos, "Neural mechanisms of audition," Physiol. Rev. , 34, 497-529 (1954). 15. G . L . Gerstein and N. Y. Kiang, "Responses of single units in the auditory cor tex," Exper. Neurol . ,

10, 1-18 (1964). 16. J_ E. Hind, "An electrophysiological determinat ion of tonoptic organization of auditory cortex of the

cat ," J. Neurophysiol . , 16, 475-489 (1953). 17. Y. KatsuI~d, T. Watanabe, and N. Maruyama, "Activity of auditory neurons in upper levels of brain

of cat ," J. Neurophysiol . , 22, 343-359 (1959). 18. P . G . Nelson and S. D. Eru lcar , "Synaptic mechanisms of excitation and inhibition in the auditory

pathway," J. Neurophysiol . , 26, 908-923 (1963). 19. D . E . Parker , "Vertical organizat ion of the auditory cortex of the cat ," T. Auditory Res . , 2, 99-124

(1962). 20. F. Reinozo-Suarez, Topographical Brain Atlas of the Cat [in German], Darmstadt (1961). 21. D. Teas and N. Kiang, "Evoked responses f rom the auditory cortex," Exper. Neurol . , 10, 91-119

(1964). 22. S . M . Walker, M. S. Baggish, D. B. Katz, C. G. Noss, B. C. Robert, and X. T. Fruong, "A sec-

ond motor area in the ce rebra l cor tex of the dog," J. Neurophysiol . , 25, 607-620 (1962). 23. J. C. Whitfield and E. F. Evans, "Responses of auditory cor tex neurons to stimuli of changing f r e -

quency," J. Neurophysiol . , 28, 655-672 (1965).

120