GABA_B-receptor-mediated inhibition reduces the orientation selectivity of the sustained response of striate cortical neurons in cats

Abstract

Blocking GABAA-receptor-mediated inhibition reduces the selectivity of striate cortical neurons for the orientation of a light bar primarily by reducing the selectivity of their onset transient (initial 200 ms) response. Blocking GABAB-receptor-mediated inhibition with phaclofen, however, is not reported to reduce the orientation selectivity of these neurons when it is measured with a light bar. We hypothesized that blocking GABAB-receptor-mediated inhibition would instead affect the orientation selectivity of cortical neurons by reducing the selectivity of their sustained response to a prolonged stimulus. To test this hypothesis, we stimulated 21 striate cortical neurons with drifting sine-wave gratings and measured their orientation selectivity before, during, and after iontophoretic injection of 2-hydroxy-saclofen (2-OH-S), a selective GABAB-receptor antagonist. 2-OH-S reduced the orientation selectivity of six of eight simple cells by an average of 28.8 (± 13.2)% and reduced the orientation selectivity of eight of 13 complex cells by an average of 32.3 (± 27.4)%. As predicted, 2-OH-S reduced the orientation selectivity of the neurons' sustained response, but did not reduce the orientation selectivity of their onset transient response. 2-OH-S also increased the length of spike “bursts” (two or more spikes with interspike intervals ≤ 8 ms) and eliminated the orientation selectivity of these bursts for six cells. These results are the first demonstration of a functional role for GABAB receptors in visual cortex and support the hypothesis that two GABA-mediated inhibitory mechanisms, one fast and the other slow, operate within the striate cortex to shape the response properties of individual neurons.

Contribution of inhibitory mechanisms to direction selectivity and response normalization in macaque middle temporal area

“…2D, which plots a time-resolved DI for the population response in the presence and absence of BMI. These findings imply that, in a subset of neurons, directional tuning during the early response period is substantially shaped by inhibition mediated through GABA A from within MT whereas, during late-response periods, either afferent inputs supply the directional information or inhibitory mechanisms other than GABA A participate in its generation (25). This finding contradicts a strictly hierarchical view in which directional tuning is simply inherited from earlier stages (13) and where MT neurons perform more complex and global computations about object and͞or ego-motion (13,26).…”

“…It is interesting to note that BMI mostly affected the early-response period whereas later periods show stronger directionality, even in the presence of BMI. A study on the contribution of GABA A vs. GABA B in shaping tuning functions has demonstrated that GABA A mostly influence the early-response component whereas the sustained response is mostly affected by GABA B (25). Based on these findings, it is tempting to speculate that neurons that are nondirectional during their earlyresponse period in the presence of BMI (a GABA A antagonist) might not regain their directionality during later response periods if baclofen (a GABA B antagonist) was also applied.…”

Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex

“…We conclude that cortical GABA A inhibition plays a minor role in the suppressive effect of the CRF surround. However, there is a report that a blockade of GABA B receptors in V1 reduces the orientation selectivity of the sustained component of visual response (Allison et al, 1996). Therefore, the contribution of slow GABA B inhibition to surround suppression remains to be clarified.…”

Different roles for GABAA and GABAB receptors in visual processing in the rat superior colliculus

“…There is ample evidence that GABAB receptors mediate slow IPSPs following the electrical stimulation of afferents to LGN X and Y cells in vitro (Soltesz, Lightowler, Leresche & Crunelli, 1989) but there have been few attempts to ascribe a function in visual processing to GABAB receptors. One recent report (Allison, Kabara, Snider, Casagrande & Bonds, 1996) suggests that GABAB receptors participate in the generation of orientation tuning in conjunction with GABAA receptors in the visual cortex. The finding that GABAB receptors are involved in response habituation is quite novel.…”