Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques

Abstract

We have previously reported that cells in cat areas 17 and 18 can show increases in response to non-optimal orientations or directions, commensurate with a loss of inhibition, during inactivation of laterally remote, visuotopically corresponding sites by iontophoresis of gamma-aminobutyric acid (GABA). We now present anatomical evidence for inhibitory projections from inactivation sites to recording sites where 'disinhibitory' effects were elicited. We made microinjections of [3H]-nipecotic acid, which selectively exploits the GABA re-uptake mechanism, < 100 microm from recording sites where cells had shown either an increase in response to non-optimal orientations during inactivation of a cross-orientation site (n = 2) or an increase in response to the non-preferred direction during inactivation of an iso-orientation site with opposite direction preference (n = 5). Retrogradely labelled GABAergic neurons were detected autoradiographically and their distribution was reconstructed from series of horizontal sections. In every case, radiolabelled cells were found in the vicinity of the inactivation site (three to six within 150 microm). The injection and inactivation sites were located in layers II/III-IV and their horizontal separation ranged from 400 to 560 microm. In another experiment, iontophoresis of biocytin at an inactivation site in layer III labelled two large basket cells with terminals in close proximity to cross-orientation recording sites in layers II/III where disinhibitory effects on orientation tuning had been elicited. We argue that the inactivation of inhibitory projections from inactivation to recording sites made a major contribution to the observed effects by reducing the strength of inhibition during non-optimal stimulation in recurrently connected excitatory neurons presynaptic to a recorded cell. The results provide further evidence that cortical orientation tuning and direction selectivity are sharpened, respectively, by cross-orientation inhibition and iso-orientation inhibition between cells with opposite direction preferences.

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

“…Our data confirm previous results demonstrating that inhibition is an important contributor to directional tuning (3,7,9). It has previously been thought that most of MT's input is highly direction selective (12,13,26).…”

“…We tested this possibility by reducing local inhibition within MT. Inhibition substantially contributes to the generation of direction selectivity in V1 (3,4,(6)(7)(8)(9). We hypothesized that MT direction selectivity should be largely unaffected by removal͞reduction of inhibition, if inherited from earlier areas, whereas direction selectivity should be substantially reduced if generated de novo within MT.…”

“…V isual motion processing has been the subject of intense research over the past decades (1)(2)(3)(4)(5)(6)(7)(8)(9)(10). In primates, directional motion selectivity in the geniculo-cortical system occurs first in primary visual cortex (V1) (e.g., see ref.…”

Predictive Coding as a Model of Response Properties in Cortical Area V1

“…In the model, blockade of inhibition from neurons with a specific orientation preference should cause neighboring prediction neurons to show increased response to that orientation, rather than simply causing a general disinhibition to all orientations. Such effects have been recorded in V1 (Crook et al, 1998), and analogous data have been obtained from cortical area TE (Wang et al, 2000). The current model is also consistent with neurophysiological evidence that the strength of lateral inhibition peaks for stimuli presented at the preferred orientation of the recorded cortical cell (Ferster, 1986;Sato et al, 1996;Sompolinsky and Shapley, 1997).…”

Local networks in visual cortex and their influence on neuronal responses and dynamics

“…Much of the evidence that has been put forth in support of recurrent models of orientation tuning comes from experiments not restricted to layer IV simple cells. For instance, it has been demonstrated that remote inactivation of orthogonal orientation columns can reduce the orientation selectivity of neurons located 350-700 lm distant [13,15]. This provides strong support for the importance of an intact cortical network for normal orientation tuning.…”