The role of gabaergic inhibition in the response properties of neurones in cat visual area 18

NeuroscienceVol. 17, No. I, pp. 49-55, 1986 Printed in Great Britain

0306-4522/86$3.00+ 0.00

PergamonPress Ltd IBRO

THE ROLE OF GABAERGIC INHIBITION RESPONSE PROPERTIES OF NEURONES VISUAL AREA 18

IN THE IN CAT

T. R. VIDYASAGAR and W. HEIDE Department of Neurobiology, Max-Planck Institute for Biophysical Chemistry, Goettingen, West Germany Abstract-Bicuculline methiodide was iontophoretically applied to single neurones in cat area 18 to investigate how removal of y-aminobutyrate mediated inhibition affects the visual response properties. Moving sinusoidal gratings were used to study spatial and temporal response characteristics. Orientation sensitivity and spatial and temporal frequency tuning curves were determined with and without iontophoretically applied bicuculline. In most neurones, orientation sensitivity and spatial frequency tuning remained largely unaffected, whereas temporal frequency tuning was very much broadened. It is suggested that the dominant excitatory input to area 18 cells is a spatially organized input from area 17 and local inhibition in area 18 sharpens primarily temporal selectivity. An alternative explanation of our results would be that the distribution of synapses mediating temporal tuning in area 18 is fundamentally different from that mediating spatial frequency and orientation tuning, which may be located at sites distant from the cell body and relatively inaccessible to the drug application.

Electrophysiological’*” and neuropharmacologiquency at a constant temporal frequency. Movshon ca126,27*29 studies have established the importance of et al.*’ have explored this question by comparing the inhibitory mechanisms for the orientation and directemporal frequency tuning of cells in areas 17 and 18 tion selectivities of neurones in the cat’s visual area and have concluded that there is a genuine difference 17. One useful line of approach has heen to remove between the two areas, with area 18 cells usually y-aminobutyrate (GABA) mediated inhibition by the showing at low temporal poorer responses microiontophoretic ejection of bicuculline in the close frequencies. To study whether GABA-mediated vicinity of the neurone being recorded.26*27,29 During inhibition plays a role in this temporal tuning of area such drug application, the orientation and direction 18 cells, we have expressed the temporal sensitivity of sensitivities of most striate cortical cells are greatly these cells in temporal frequencies instead of in reduced. We have employed the same approach to angular velocities and investigated the changes during examine the role of GABAergic inhibition in some of the iontophoretic application of bicuculline. The the response properties of cells in area 18. Our findings have been reported in a preliminary form.3’ interest in area 18 takes note of the fact that it EXPERIMENTALPROCEDURES receives a visual input from area 176~8~13~L4J2 as well as a direct input from the lateral geniculate nucleus.4~7*9~23General We recorded the responses to different orienCats were anaesthetized with 25mg/kg of ketamine tations, spatial frequencies and temporal frequencies (Parke-Davis) for the initial surgery and later maintained on a (70: 30) nitrous oxide:oxygen mixture and 1 mg/kg/h of a moving sine wave grating before and during pentobarbital (Nembutal; CEVA). The operative iontophoretic administration of bicuculline methiprocedures consisted of venous and tracheal canulations, odide. While both area 17 and area 18 neurones show bilateral cervical sympathectomy and a craniotomy. The comparable orientation sensitivities,‘*v13 their spatial animals were paralysed with 5 mg/kg/h of gallamine triethand temporal frequency selectivities differ iodide (Sigma) and 0.1 mg/kg/h of pancuronium (Organon markedly.*’ Area 17 cells have a broad range of Teknika), and artificially ventilated keeping the end-tidal CO, near 4%. Atropine and phenylephrine (Neosynephrine) preferred spatial frequencies, whereas all area 18 (Ursapharm) were topically applied on the eyes and 3 mm neurones are tuned to relatively coarse spatial fre- diameter artificial pupils were used. Hard contact lenses quencies. It is well known that area 18 neurones were used to correct refraction and to bring images at 57 cm prefer higher angular velocities than do area 17 cells, to focus on the retina. Subscapular temperature was when stimulated with bars or edges.3J9~22~28 But this maintained at 38°C with a heating pad. For recording from area 18, the electrode penetration was difference might just he related to the fact that area usually anterior to Horsley-Clark coordinate Al and at least 18 neurones generally prefer coarser spatial fre- 2 mm from the midline. The majority of the receptive fields were located between 5 and 10” from the centre of area quencies, since the angular velocity of a moving grating is inversely proportional to its spatial fre- centralis, and between 2 and 5” from the vertical meridian. Abbreviations: GABA, y-aminobutyrate;

In a few instances, oblique penetrations were made across the vertical meridian passing from area 17 to area 18. Area 17 recordings were otherwise mostly done in the medial bank of the lateral sulcus and around Horsley-Clark coordi-

LGN, lateral

geniculate nucleus. 49

so

1‘. K.

VIDYASAGAH aRd W. HEIIE

nates PS, L1. Data from area I7 will be reported separately and are cited here only for comparison. Each penetration was marked by one or more electrolytic lesions and the recording sites were reconstructed in 52 micrometer Nissl stained sections by referring the lesions to the micrometer readings. Application of bicuculline For recording single units and for iontophoresis of drugs, an electrode assembly was used that had a central tungstenin-glass microelectrode around which were glued a number of micropipettes. Each of the pipettes was filled with one of the following solutions: bicuculline methiodide (Pierce) 0.01 M in I65 mM NaCl, pH 3; L-glutamic acid (Sigma) 0.5 M, pH 8; GABA (Sigma) 0.5 M, pH 3; NaCl 3 M. The pharmacological effectiveness of the bicuculline was assessed by its ability to nullify the inhibitory effect of GABA on the responses of the neurone. The currents of bicuculline that we used were usually sufficient to block iontophoretic GABA ejected at currents that were even three or four times those necessary to completely suppress the unit’s response to an optimal stimulus. In most cases, we have tried recording at the highest currents of bicuculline that were possible to apply without producing high spontaneous activity and bursting responses. For further details of the iontophoretic technique and controls. see a preceding paper.” Visual stimulation The visual stimuli were produced on a cathode ray scope (Joyce Electronics Ltd, Cambridge, England) using a microprocessor (CMS Cambridge, England) The Screen had a mean luminance of 200 cd/m’ and subtended 31 x 22” of visual angle. For each Parameter (spatial frequency, orientation or temporal frequency) a PDP-I I computer controlled the presentation of the different moving sine wave gratings in an interleaved fashion and recorded the peristimulus time histograms. Near-optimum values were chosen for the two invariant parameters. The contrasts [(L,, - &,)I(&._ + &,,)I used were usually between 0.1 and 0.5. Response amplitude to a fixed suprathreshold contrast was usually used to make the tuning curves. Contrast sensitivity measurements were rarely done, since optimal spatial frequency and spatial frequency tuning band-width are not very different between sensitivity and response amplitude determinations.m Orientation tuning has also been shown to be independent of contrast in area 17.‘“34We also observed with area 18 neurones that these parameters were largely indepcndent of contrast. However, we took care not to use very high contrasts that can produce saturation effects, especially with the higher rates of discharge under bicuculline.

RESULTS

General Cells were classified’0*‘5 using moving light and dark bars and edges produced on the catbode ray scope. Our sample of fifty area 18 neurones consisted of 33 complex cells, 14 simple cells and three A celk.

Cells in area 18 show varying degrees of endinhibition. But we ahvays used long stimuli (subtending at least 10” in the long axis of the receptive fieM) and have excluded hyparcomplex ceils from our study. No B cells were encountered in area 18. Complex cells respondal to low spa&l fmquewics with a modulated discharge, while at higher frequencies they showed an unmodulated increase in

firing. For thcsc cells. the net incrcasc in impulse rate above the spontaneous activity level was used IO calculate the tuning curves. For simple cellb. the response usually remained modulated at all spatial frequencies. For these, each peristimulus time histogram was analysed into its Fourier component\ and the amplitude of the first (fundamental) harmonic component was taken as a measure of the cell’s response in order to calculate the tuning curves. Since in most cases there was no significant reduction in the degree of modulation on application of bicuculline. the first harmonic component was again used as the measure of response. The ratio of the amplitudes of the response components at the fundamental frequency u,) and the zero frequency (J,) (first to zero ratio) is considered to be a good measure of the degree to which a neuron’s response consists of modulated and unmodulated components.Z0 For two simple cells and all three A ceils. the unmodulated component (fo) dominated the response for the control and/or bicuculline conditions, with a first to zero ratio less than one. In these cases. the change in .1;, component was taken as the response measure. Effect qf bicuculline application

on urea I8 nrurones

Figure I shows the response of a typical area I8 complex cell to moving sine wave gratings, and the changes accompanying iontophoretic ejection of bicuculline methiodide. It can be seen that removal of GABAergic inhibition had little effect on the cell’s orientation selectivity or spatial frequency tuning. Even though the response at the optimum orientation and best spatial frequency was considerably greater, there was no comparable increase at the nonoptimum orientations and spatial frequencies. However, the response attenuation at low temporal frequencies, which is a characteristic feature of area I8 neurones,” is abolished during the administration of bicuculline. We have made the peristimulus time histograms for the different temporal frequencies visually comparable by keeping the analysis time (binwidth x number of sweeps) constant while changing the bin-width to display the same number of cycles per sweep for all drift frequencies. The temporal frequency tuning curve assumes a near low-pass characteristic typical of most lateral geniculate nucleus (LGN)” and area 17” cells. Figure 2A shows another area I8 cell whose spatial frequency and orientation tuning curves were not affected by the application of bicuculline, whereas the temporal frequency tuning again became markedly broader. It can also be seen that the iontophoretic application of the excitatory transmitter, glutamate did not achieve any broadening, indicating that the temporal frequency sharpening is mediated by specific GABAergic inhibition. Even though contrast sensitivity measures were not routinely done. the change in temporal frequency tuning was also seen equally well at lower contrasts. It is also noteworthy that the cell in Fig. 1 shows little increase in spontaneous activity

51

GABAergic inhibition in cat area 18

ORIENTATION

TUNING

CONTROL

zY

WITH

BICUCULLINE

WITH

BICUCULLINE

ii

TEMPORAL

FREQUENCY

TUNING

CONTROL

WITH

BICUCULLINE

TF:O.LHz 01 z

0.2 TIME

ISECI

Fig. 1. Responses of a complex cell in area 18 with and without iontophoretic application of bicuculline methiodide. Post-stimulus time histograms (PSTHs) are shown on the left and normalized tuning curves on the right. The total counts of spikes shown above each PSTH are comparable between PSTHs belonging to the same tuning curve, e.g. control orientation tuning curve, but not between PSTHs of two different tuning curves, e.g. between control and bicuculline orientation tuning curves, since the total analysis time was not always the same between different tuning curves. For an absolute comparison, see the ordinate which has been scaled appropriately for each set of PSTHs. Total number of bins in each PSTH: 200. The arrows above the PSTHs for orientation tuning indicate the direction of movement which was always orthogonal to the long axis of the grating. For orientation and spatial frequency tuning measurements, a temporal frequency of 1.6 Hz was used. The spatial frequency used for measuring the orientation and temporal frequency selectivities was 0.1 cyc/deg. The optimal orientation (see top tuning curve) was used for the spatial and temporal tuning measurements. Contrast in all cases was 0.5. The iontophoretic current was 4OnA. The levels of spontaneous activity with and without bicuculline are shown with the temporal frequency tuning responses (WONT.). SF, spatial frequency; TF, temporal frequency. with bicuculline, but nevertheless exhibits a clear broadening of temporal tuning. It is further unlikely that some response saturation at high contrast caused this change, since any such saturation would have had some effect on the other tuning curves. Even

though the bicuculline could nullify the effects of even relatively high currents of locally iontophoresed GABA,

it is still possible

that

the drug could

not

reach distal inhibitory synapses. In most cases, we have increased the duration of drug application and

5’ _&

T.

R. VIDYASAGAWand W. HEIDE

1

.

BICUCULLINE

:q

0 005 SPATIAL

1

01 FREQUENCY

I CYC / DEG )

1111111I 0.5 1 TEMPORAL

10 FREQUENCY

I.5

90

IHz)

Fig. 2. Normalized tuning curves for spatial frequency (left). temporal frequency (right), for an area 18 complex cell (A) and an area 17 complex cell (It), with of bicuculline methiodide. A glutamate control and a recovery curve are also frequency response of the first cell, which showed significant broadening current magnitudes in an attempt to inactivate these synapses. Nevertheless, it was generally not possible to significantly affect the orientation and spatial frequency tuning characteristics. Figure 3 pools the results for all the 50 cells we recorded from area 18. The degree of spatial broadening was limited for most cells, with only a few

180

225

270

315

360

I OEGl

(middle) and orientation and without application shown for the temporal with bicuculline.

showing marked broadening. On the other hand, for temporal tuning, lack of broadening was seen only in a small number of cells, most cells exhibiting considerable increases in tuning band-width with the application of bicuculline. Sixteen of the 50 ceils assumed nearly low-pass profiles. The mean control spatial frequency band-width (measured as full width TEMPORAL

SPATIAL FREQUENCY

135

ORIENTATION

FREOUE

ORIENTATION

NCY

N=50

CHANGE OF TUNfNG WIDTH Fig. 3. Increase in tuning width with iontophoretic application of bicuculhne methiodide. Stippled areas represent simple and A cells, and the rest complex cells. See text for further details.

53

GABAergic inhibition in cat area 18 in octaves at half maximum response) was 1.95 + 0.85 octaves (n = 50) and with bicuculhne the mean increased 20% to 2.32 + 1.04. For temporal frequency tuning the change was 82% from 3.12 + 1.04 to 5.66 + 2.7 octaves. For cells showing low-pass tuning profiles with bicuculline, a bandwidth three times that of the control mean was taken to calculate the mean band-width. The mean orientation tuning (half-width in degrees at half maximum response) increased by 34% from 29” k 11.5” to 39” + 20”. It should be appreciated that this is a very small degree of broadening in comparison to the potential change that can occur and to the change that does occur in area 17. Our orientation tuning values might have been slightly over-estimated, since the tuning curves were usually done in 45” steps to save time. There was a strong tendency for orientation tuning and spatial frequency tuning to be similarly influenced by bicuculline+either both becoming broader, or neither being affected. Further, the cells which showed broadening of tuning for these spatial parameters, usually exhibited broadening of temporal tuning as well. There were not striking differences between simple and complex cells in the overall picture. Direction sensitivity was calculated for responses before and during application of bicuculline according to the following formula: Direction sensitivity index = Response in the preferred direction - Resnonse in the onoosite direction _. Response in the preferred direction ’ The mean control index was 0.76 (SD f 0.26), denoting a considerable degree of directional selectivity. On applying bicuculline, cells lost their direction sensitivities to varying degrees, with an average index of 0.59 (SD + 0.32). A few cells lost their direction sensitivities almost entirely, but a large number of neurones showed only mild or moderate changes. There was no strict correlation between changes in directional and orientational sensitivities, except in cells whose orientation sensitivities were almost abolished by the bicuculline. Often there was a significant loss of directional sensitivity with little change in spatial frequency or orientation tuning. For 38 of the 50 cells, histology could confirm the laminar position. For the rest, we could only confirm that they were within area 18, but not their laminar distribution. We recorded from five cells (four simple and one complex) in layer IV, 16 in layers II and III, and 17 in layers V and VI. In this limited histological data, we did not notice any appreciable laminar differences. Of the five layer IV cells, temporal frequency tuning became very broad in two cells and showed at least 50% broadening in two others; but only one of these cells lost its orientation sensitivity to a significant degree. Spatial frequency tuning

remained unaffected in three cells and showed close to 50% broadening in the other two. The changes seen in area 18 are however quite different from what typically occurs with an area 17 neurone upon iontophoretic application of bicuculline. It is already well established that with most area 17 cells orientation and direction sensitivities are diminished when GABA inhibition is removed.26T27*29 Figure 2B shows for comparison one of the 21 cells we recorded from area 17. In this case, ejection of bicuculline brought about marked broadening of all three tuning curves. Unlike area 18, most striate neurones in the cat do not show much low temporal frequency attenuation;2’ but whenever a certain degree of such attenuation was present (as in Fig. 2B), we have noticed that it could be reduced by application of bicuculline. However, in contrast to area 18, by far the major change seen in area 17 is with the spatial properties. DlSCUSSlON

Our iontophoretic experiments show that GABAergic inhibition in area 18 sharpens mainly temporal response characteristics, and is much less responsible for the spatial frequency and orientation selectivities. While orientation and spatial frequency selectivities are the striking transformations achieved between LGN and area 17, area 18 neurones are remarkable for their temporal selectivity in comparison to area 17 neurones.” It appears that local inhibition in area 18 is concerned largely with this temporal property. It is however possible that we have mainly recorded from second order cells that get a spatially organized input from first order cells in area 18 whose spatial and orientation selectivities are indeed organized by local inhibition. But this interpretation cannot be supported by our data from the limited number of lamina IV cells. Further, the existence of a second inhibitory transmitter for spatial properties cannot be excluded; but it is unlikely because of the lack of evidence for such a transmitter in the visual cortex. There is however the possibility that the synapses mediating temporal frequency dependent effects are more accessible to the drug than those mediating spatially dependent effects. For example, the former may be located on and close to the cell body, whereas the latter may be more distally located. Such a distribution of synapses on area 18 neurones would then be a surprising difference from the synaptic organization in area 17, where comparable iontophoretic application of bicuculline frequently led to significant losses of spatial frequency and orientation selectivities. If we assume that the excitatory input provides all the spatial selectivity, one possibility is a direct convergent excitatory input from LGN of the type originally proposed ty Hubel and Wiesel for area 17i2 bestowing the spatial tuning. However, such a scheme for orientation sensitivity in area 17 has been heavily

54

T. R. VIDYASAGAR and W. HEIDE

even though this does not ipso jhcto make it unlikely for area 18. The other possibility is that the dominant excitatory input for an area 18 cell comes not from the LGN, but rather from area 17, as in the hierarchical model first proposed by Hubel and Wiesel.” Thus the incoming information could be already totally organized as far as its spatial aspects are concerned and the local inhibition in area 18 may sharpen only the temporal tuning. The reports on the effect of lesioning or cooling area 17 on the response properties of area 18 neurones are inconclusive. In one study,2 after chronic lesions of area 17, half the cells in area 18 were unresponsive and those that could be visually driven exhibited much poorer stimulus specificities. But in two other studies, one using acute lesions3 and the other reversible cooling of area 17,25the changes seen were less drastic. That appreciable changes were seen only infrequently with these procedures may be related to the formidable technical problems involved in reliably inactivating area 17 alone without affecting area 18 neurones. Because of the proximity of the two areas, any procedure that leaves area 18 neurones functioning might not have sufficiently reduced the activity of the corresponding area 17 neurones. One difficulty with the suggestion that the area 17 disputed,1.16.26.27.29

input may be the more dominant excitatory input to area 18 is the fact that the spectra of optimal spatial frequencies for areas 17 and 18 show only a very limited overlap. ” Nevertheless it is not inconsistent with the finding that only certain clusters of neurones in the supragranular layers of area 17 project to area 18.8 This subclass of cells may be those tuned to the lowest spatial frequencies and providing the primary excitatory input to area 18, with the direct geniculate afferents performing a subsidiary role. This hierarchical scheme for the cat visual system gains indirect support from a recent finding in the monkey.’ Despite the sparse evidence for a direct geniculate input to the monkey prestriate area, a comparison of the spatial and temporal frequency selectivities of cells in Vl and V2 revealed differences between the two areas very similar to those in the cat. This finding suggests that at least in the monkey, the spatiotemporal differences between areas 17 and 18 can exist in the absence of a significant direct LGN input to area 18. Unless the extrageniculate subcortical input to area 1833should turn out to be important, this points to area 17 as the source of the major input to area 18. Acknowledgements-We

thank Prof. 0. D. Creutzfeldt and Dr B. B. Lee for helpful criticism, and Mrs U. Steveling and Mrs E. Nicksch for histological assistance.

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