Mechanisms underlying orientation selectivity of neurons in the primary visual cortex of the macaque.

Abstract

1. Effects of blocking intracortical inhibition by microiontophoretic administration of bicuculline methiodide (BMI), a selective antagonist for GABAA receptors, on orientation selectivity of 109 neurones were studied in the primary visual cortex (V1) of anaesthetized and paralysed monkeys. 2. The averaged orientation tuning of visual responses of cells was poor in cytochrome oxidaserich blobs of layer II/III and in layer IVc/J, moderate in layers IVb, IVca and V, and sharp in the interblob region of layer II/III and in layers IVa and VI. 3. Iontophoretic administration of BMI reduced the sharpness of orientation tuning of cells to a varying extent in each layer. In most cells, furthermore, the originally ineffective stimuli induced visual responses during the BMI administration, suggesting that excitatory inputs evoked by the non-optimally oriented stimuli were masked by GABAergic inhibition. Nevertheless, the maximal facilitation was observed in the response to the optimally or near-optimally oriented stimuli. 4. There was a difference in such an effect of BMI among layers. Orientation selectivity of cells in interblobs in layer II/III and in layer IVb was sensitive to BMI whereas that of cells in layer VI was relatively insensitive to BMI, suggesting a larger contribution of excitatory mechanisms to the orientation selectivity in this layer. 5. In the orientation-selective cells, an analysis of the magnitude of excitation and inhibition evoked by stimuli at various orientations suggests that both inputs tune around the optimal orientation and their magnitudes are almost proportional to each other except at the optimal orientation. This analysis also indicates that the orientation tuning of inhibition had a less prominent peak around the optimal orientation than that of excitation. This dominance of excitation over inhibition around the optimal orientation may function to accentuate the response to the optimally oriented stimulus.6. These results suggest that, in the monkey Vi, the orientation selectivity of cells is largely dependent on the orientation-biased excitatory and inhibitory inputs which have a broader tuning profile, covering from the optimal to null-orientation, than that observed in extracellularly recorded responses at the control level.

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

“…This is also consistent with evidence that blocking inhibitory effects across a local population of cortical cells greatly reduces orientation selectivity (Sillito, 1975;Tsumoto et al, 1979;Sato et al, 1996). 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). In the model, the strength of inhibition between any two prediction neurons is proportional to the degree of overlap between the RFs.…”

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

“…There is also evidence that the influence of inhibition on orientation tuning in monkey V1 depends strongly on layer. Sato et al [57] found that the broadening of orientation tuning that results from local iontophoresis of GABA antagonists was strongest outside of the input layers. Thus, orientation tuning may be re-computed in different cortical layers, by use of different synaptic integration mechanisms.…”

Untuned Suppression Makes a Major Contribution to the Enhancement of Orientation Selectivity in Macaque V1

“…However, feedforward excitation alone cannot provide the suppression of responses to nonpreferred orientations that has been observed (De Valois et al, 1982;Celebrini et al, 1993;Ringach et al, 2002b). To account for orientation selectivity, theorists have proposed corticocortical amplification (Ben-Yishai et al, 1995;Somers et al, 1995;Mariño et al, 2005), corticocortical inhibition (Sato et al, 1996;Troyer et al, 1998;McLaughlin et al, 2000;Monier et al, 2003), and presynaptic depression Freeman et al, 2002). Many experimental studies (Nelson and Frost, 1978;Sillito et al, 1980;Bonds, 1989;Volgushev et al, 1993;Sato et al, 1996;Ringach et al, 2002a,b;Shapley et al, 2003) concluded that suppressive or inhibitory cortical mechanisms were involved.…”