Flash evoked responses in a song control nucleus of the zebra finch (Taeniopygia guttata castanotis)

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B R E 20605

Flash evoked responses in a song control nucleus.of the zebra finch (Taeniopygia guttata castanotis)

H A N S - J O A C H I M B I S C H O F and J U R G E N E N G E L A G E

University of Bielefeld. Department ~f Ethology, P. O. Box 8040. D-4800 Bieleteld. (F. R. (;.) (Accepted S e p t e m b e r 17th. 1984 I

Key words': zebra finch visually evoked potentials h y p e r s t n a t u m ventrale pars caudale

The song of the zebra finch is facilitated and altered bv the presence ol a female. Thus. visual information s h o u l d affect the song system of the bird. Visually e v o k e d potentials can be recorded from n. hyperstriatum ventrale pars caudale [HVc). T h e long latency ot this potential and its variability indicate several processing steps between primary sensory areas of the telencephalon and H V C . With- in H V c , u n d e r t h e s e e x p e r i m e n t a l conditions no interaction between acoustic and visual input could be d e m o n s t r a t e d . However. at the dorsal border and within the shelf below HVc. visual information s e e m s to e n h a n c e acoustically e v o k e d potentials

The song of oscine birds is c o n t r o l l e d bv a well-de- fined system of c o n c a t e n a t e d brain nuclei, the so- called song system L3. A s f e e d b a c k control is nec- essary for d e v e l o p m e n t and for p e r f o r m a n c e of song in m a n y of these birds s, c o n n e c t i o n s from the auditory system to the song control system have been pro- posed and could be d e m o n s t r a t e d bv several authors 5 7.1o, i],14. A c c o r d i n g to their results, the nucleus h y p e r s t r i a t u m v e n t r a l e pars c a u d a l e ( H V c ) receives input from field L, the t e l e n c e p h a l i c nucleus of the auditory p a t h w a y in the b i r d ' s brain.

The song of the m a l e is, at least in the z e b r a finch.

facilitated by the p r e s e n c e o f a female. II could be d e m o n s t r a t e d that quality and q u a n t i t y of the m a l e ' s song is a l t e r e d by p r e s e n t a t i o n of a living female as well as by a f e m a l e d u m m y o r even a picture of a female 1-4. W i t h increasing similarity of the stimulus to a living female the song of the male b e c o m e s m o r e s t e r e o t y p e d and f r e q u e n t and has m o r e i n t r o d u c t o r y elements and motifs. B a s e d on these song features.

two different song types can be d e t e c t e d u n d e r natural conditions: the so-called 'undirected" song which is u t t e r e d in situations not d e a r l y assoctated with a definite function; and the ' d i r e c t e d ' song, which is directed t o w a r d s the f e m a l e and c o m b i n e d with court- ship display 4-12,15. Solely acoustic contact with a female is not sufficient to elicit c o u r t s h i p b e h a v i o r and directed song (Bischof, u n p u b l i s h e d results).

F r o m these b e h a v i o r a l studies it is likely that the

song control system is in some way affected by visual information. H o w e v e r . there are no data available concerning c o n n e c t i o n s b e t w e e n the visual system and song control nuclei. Thus we d e c i d e d to e x a m i n e directly w h e t h e r the song system receives visual input. F o r this p u r p o s e , we tried to r e c o r d visually e v o k e d potentials ( V E P s ) from HVc. while one of the b i r d ' s eyes was s t i m u l a t e d with flashes.

HVc. a higher o r d e r nucleus of the song control system, was chosen, b e c a u s e it receives acoustic input (see aboveJ. W e p r o p o s e d that most likely acoustic and visual influences s h o u l d interact for the control of song elicitation. E v o k e d potentials were re- c o r d e d with glass e l e c t r o d e s (K-citrate 1 0 - 4 0 M Q ) from the HVc of 20 adult male z e b r a finches. T h e birds were a n e s t h e t i z e d with U r e t h a n e (20% w~v.

U.1 mlJ. Visual stimuli were p r o v i d e d by a s t r o b o - scope; the flash was d i r e c t e d to the c o n t r a l a t e r a l eye by a fiber-optic system. Clicks were gwen as an acoustic stimulus by e a r p h o n e s c o n n e c t e d to the hol- low e a r b a r s by 2 cm length of very flexible vinyl tub- ing. T h r e e different c o m b i n a t i o n s of stimuli were used t h r o u g h o u t the e x p e r i m e n t s : c o n t r a l a t e r a l acoustic stimulation, c o n t r a l a t e r a l visual s t i m u l a t i o n and a c o m b i n a t i o n of both, In addition controls were m a d e by disconnecting the e a r p h o n e s f r o m the ear- bars and d i s p l a c e m e n t of the fiber optics or simply switching off the triggers.

The signals were usually a v e r a g e d 64 times bv a

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Fig. 1. Averaged c~oked potentials recorded from the l-]Vc region. Left, acoustic stimulation: middle, visual stinmlation: right, combined ,timulmion. Average 64x, bin width 500 us. Arrows: I. VEP: 2. parts within the recordings, where xisual and acoustic stimuli ma\ interact (scc tcxt), st, stimulus.

Nicolet signal averager. Storing and processing of the data was accomplished by a HP-85 microcomputer.

This device also triggered the different stimuli and controlled the experimental procedure.

Besides very slow potential shifts of large amplitude, x~hich can be seen in recordings throughout the brain and which were eliminated by a high pass filter with a cut-off frequency of 5 Hz, faster fluctuations of large amplitude were detected within the HVc area, when the bird was not stimulated either visually or acousticalh'. Most of these large shifts disap- peared with the application of stimuli. However,

proper registration of averaged evoked potentials was very difficult due to the fact that one of these large asynchronous potentials could distort an average curve essentially, Thus. it was carefulJv detected throughout the experiments whether potentials de- veloped stepwise in the course of the average procedure or whether they appeared as the result of one sweep.

With acoustic stimulation, a sharp n e g a t i v e - p o s i - tive wave occurred with a peak l a t c n c \ of 25 ms for the negative potential and a duration of about 15 ms.

The shape and latency of this potential did not change

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essentially during its o c c u r r e n c e b e t w e e n 100 and 1000/*m of d e p t h as m e a s u r e d from the surface of the brain (Fig. 1).

These latencies are consistent with those of single cell recordings for acoustic n e u r o n s within the H V c area,~.~. ~c~.

The a m p l i t u d e of the first negative p o t e n t i a l in- creased b e t w e e n 100 and 2 0 0 / t i n and d e c r e a s e d from 700 to 900 ~ m of d e p t h ; h o w e v e r , it could be detected down to a d e p t h of a b o u t 20(1(]/tin. Kelly and N o t t e b o h m 7 s t a t e d that HVc has an underlying shelf of acoustic neurons. This was c o n f i r m e d by the studies of Katz and Gurney~ and Margoliashl~L and is consistent with our finding that the acoustic influence ~s strongest at the ventral b o r d e r of HVc (Fig. 2 A L

With visual stimulation, a negative p o t e n t i a l occurred from a b o u t 200 to 700 u m from the surface.

Peak latency was about 140 ms, the duration of the wave about 100 ms (Fig~. 1, 2). Thus. in contrast to the acoustically e v o k e d p o t e n t i a l which could be recorded even outside the nucleus, the VEP was re- stricted to the area of HVc, The a m p l i t u d e o t the VEP is lower than that of the acoustic p o t e n t i a l , the shape seems to be m o r e variable.

If both stimuli were c o m b i n e d , the potentials de- scribed above a p p e a r e d s i m u l t a n e o u s l y in the upper part of the recordings. The resulting w a v e f o r m was apparently a s u m m a t i o n of the two single ew~ked potentials. If one s u p e r i m p o s e s the two s e p a r a t e recordings of visually and acoustically e v o k e d p o t e n - tials bv the c o m p u t e r , the same waveform as with double stimulation results (Fig. 3),

However. this s t a t e m e n t holds true only for zt depth from about 21J0 to 701) urn. the a r e a where pure

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Fig. 3. Means of 5 recordings from a depth between 200 and 7{)(I #m to demonstrate the main leatures of the responses to different stimuli within HVc. Comb. av. recordings of pure acoustic or visual stimulations are added by the computer. Nole the similarity to the curve of combined stimulation.

optic influence can be d e t e c t e d . A t the ventral border of HVc and within the shelf region below the nucleus, the c o m b i n a t i o n of stimuli resulted in an en- hanced second negative u a v e if c o m p a r e d with pure acoustic stimulation (Figs. 1,2), although with solely visual stimulation no e v o k e d potential is to be detected.

A c c o r d i n g to the anatomical findings, one can con- clude from our results that the acoustic input to HVc derives from field L of the n e o s t r i a t u m . In o t h e r experiments ( E n g e l a g e and Bischof, in p r e p a r a t i o n ) we recorded field L p e a k latencies from 10 to about 30 ms: the earliest waves may well be the trigger for the HVc potentials with a latency of 2 0 - 2 5 ms.

Again this is in g o o d a g r e e m e n t with previous studies of other authors ",'~,>.

The large latency of the V E P (135-145 ms) makes it impossible to decide which of the two visual path-

ways provides the input to HVc. The shortest latencies of VEPs in the e c t o s t r i a t u m , the telencephalic part of the tectofugal p a t h w a y , were recorded al about 40 ms. Within the Wulst, the telencephalic region of the thalamofugal tract, shortest latencies were even at about 3 0 - 3 5 ms (unpublished results).

As there is no direct connection d e m o n s t r a t e d between HVc and visual pathways, we p r o p o s e that ad- ditional regions of the t e l e n c e p h a l o n may be in- volved in the processing of visual information before it reaches HVc. Two features of our results m a k e such a proposition likely. Firsl, the c o m p a r a b l y large latency cannot be solely a result of long fiber tracts.

For example, the distance of the visual Wulst from the optic nerve is not much shorter than that of HVc.

Secondly, the shape of the VI~P in t t V c is not very sharp, perhaps as the result of a some processing steps which may desynchronize the neuronal activity elicited by light flashes.

A p p a r e n t l y , within the more dorsal parts of HVc, there is no interaction between visual and acoustic in- puts. If they are c o m b i n e d , the resulting waveform is primarily an addition of the two singly e v o k e d wave- forms. A t the ventral b o r d e r of the nucleus and the underlying shelf region, however, an interaction is very likely. Here it seems as if visual mpnt facilitates acoustic input: the visual input, although no m o r e de- tectable itself, enhances the reaction to the acoustic input. One has to consider that these results were ob- tained under anesthesia. This may sevcreh' influence the p a t t e r n of interaction between the two stimuli.

However, it is more likely that an e n h a n c e m e n t and not a diminution of interaction x~ould be found in awake animals and with m o r e natural slimulation.

O t h e r , more c o m p l i c a t e d interactions may occur in addition in n o n - a n e s t h e t i z e d p r e p a r a t i o n s . Like- wise, o t h e r stimulus programs as different spacing of the stimuli mav reveal more information about the nature of interaction at this neuronal levcl, t t o w e v e r . our results clearly d e m o n s t r a t e that there is \ isual input to HVc: w h e t h e r this input really has the function we can observe in our behavioral studies, that is to fa- cilitate the action of the nucleus and lhc o u t p u t of song, remains open to further research.

O u r thanks are due to Mrs. Kdda (icissler for her assistance in p r e p a r i n g the figures. This research was s u p p o r t e d bv the Deutsche F o r s c h u n g s g e m e i n s c h a f t (Bi 245/3).

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