Takafumi Akasaki

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

In the primary visual cortex (V1), the single-neuron response to a grating stimulus placed in the classical receptive field (CRF) is suppressed by a similar stimulus presented in the CRF surround. To assess the input mechanism underlying the surround suppression, we tested the effects of iontophoretically administered GABAA-receptor antagonist, bicuculline methiodide (BMI), for the 46 V1 neurons in anesthetized cats. First, the stimulus-size tuning curves were studied, with or without BMI administration, for each neuron by changing the size of the grating patch. During the BMI administration, the shape of the normalized size tuning curve did not change considerably. Second, the dependency of surround suppression on the orientation of the surround grating was examined. In the control, the surround suppression showed the clear orientation tuning that peaked at an orientation the same as the optimal orientation of the CRF response. The BMI administration did not change the orientation dependency of surround suppression. We also estimated the relative contribution of excitation and inhibition to the size and orientation tuning of surround suppression. It was concluded that cortical excitation and inhibition were well balanced, having similar tuning profiles for both stimulus size and orientation of the surround grating. Furthermore, surround stimuli used for V1 neurons suppressed the CRF response of neurons in the lateral geniculate nucleus. These results suggest that surround suppression is not primarily attributable to the intracortical inhibition, but because of a reduction of thalamocortical inputs, which drive the cortical excitation and inhibition, and a subsequent decrease in the cortical excitatory interactions.

Suppressive effects of receptive field surround on neuronal activity in the cat primary visual cortex.

Effects of sinusoidal grating stimulus presented outside the classical receptive field (CRF) on neuronal responses were studied in the primary visual cortex of anaesthetized cats. Among 101 cells electrophysiologically recorded, the predominant effect of the stimulus in the receptive field surround (SRF) was the suppression of responses to the CRF stimulation, and the SRF grating suppressed them up to 56% of the responses (44% suppression) to the CRF stimulus alone. The strong suppression was observed more often in layer II/III cells than in other layers and in complex cells more often than in simple cells. The modulatory effects by SRF stimulus might be enhanced by the cortical recurrent excitation particularly in the superficial layers. We also examined whether the modulation by the surround grating exhibits a differential effect according to the presence or absence of figure-ground segregation in the stimulus configuration. For this purpose, effects of stimulus configuration with orientation-, direction-contrast or relative spatial phase difference between CRF and SRF stimuli (figure-ground segregated configuration) were compared with those of uniform configuration of stimulus (non-segregated configuration). There was a population of cells, which exhibited significantly stronger suppression with non-segregated configuration than with figure-ground segregated configuration. Such differential modulation of response by the SRF stimulus in the primary visual cortex is a possible basis of perceptual figure-ground segregation.

Enriched Expression of Serotonin 1B and 2A Receptor Genes in Macaque Visual Cortex and their Bidirectional Modulatory Effects on Neuronal Responses

To study the molecular mechanism how cortical areas are specialized in adult primates, we searched for area-specific genes in macaque monkeys and found striking enrichment of serotonin (5-hydroxytryptamine, 5-HT) 1B receptor mRNA, and to a lesser extent, of 5-HT2A receptor mRNA, in the primary visual area (V1). In situ hybridization analyses revealed that both mRNA species were highly concentrated in the geniculorecipient layers IVA and IVC, where they were coexpressed in the same neurons. Monocular inactivation by tetrodotoxin injection resulted in a strong and rapid (<3 h) downregulation of these mRNAs, suggesting the retinal activity dependency of their expression. Consistent with the high expression level in V1, clear modulatory effects of 5-HT1B and 5-HT2A receptor agonists on the responses of V1 neurons were observed in in vivo electrophysiological experiments. The modulatory effect of the 5-HT1B agonist was dependent on the firing rate of the recorded neurons: The effect tended to be facilitative for neurons with a high firing rate, and suppressive for those with a low firing rate. The 5-HT2A agonist showed opposite effects. These results suggest that this serotonergic system controls the visual response in V1 for optimization of information processing toward the incoming visual inputs.

Contrast‐dependent, contextual response modulation in primary visual cortex and lateral geniculate nucleus of the cat

In the primary visual cortex (V1), the responses of neurons to stimuli presented in their classical receptive fields (CRFs) are modulated by another stimulus concurrently presented in their surround (receptive field surround, SRF). We studied the nature of the modulatory effects of SRF stimulation with respect to stimulus contrast in cat V1. In 51 V1 neurons studied, large SRF stimuli (40° × 30°) induced only the suppression of responses to CRF stimulation and the suppressive effects became stronger as the contrast for SRF stimulation increased. The contrast sensitivity of SRF suppression did not correlate with that of CRF responses. By independently controlling contrast of CRF and SRF stimuli, we studied whether SRF effects vary with CRF response magnitude. Increasing contrast for CRF stimulation caused an upward shift of the range of effective contrasts for SRF stimulation, indicating that a high contrast for SRF stimulation is required for suppressing strong responses to CRF stimulation at high contrasts. To assess the possible origin of the suppressive SRF effect on V1 neurons, we also investigated the contrast dependency of SRF effects in 28 neurons from the lateral geniculate nucleus. Our results suggest that SRF effects obtained at the subcortical level strongly contribute to those in V1. Taken together, we conclude that along the thalamocortical projections, SRF modulation exhibits a gain‐control mechanism that scales the suppressive SRF effect depending on the contrast for CRF stimulation. In addition, SRF effects can be facilitatory at low stimulus contrasts potentially due to the enlargement of the summation field.

Cross-correlation study of network dynamics in the cat primary visual cortex

To assess the network dynamics in the primary visual cortex, we performed simultaneous recordings of neuronal activity from cell pairs within 1 mm apart in anesthetized and paralyzed cats. Cross-correlograms (CCs) were calculated for the responses to grating stimuli with varying orientations and sizes for the 30 cell pairs to date. There were three patterns of cell pairs in respect of tuning property to stimulus sizes. First, both cells exhibited strong suppression of firings with stimuli larger than their classical receptive field (CRF). Second, only one cell exhibited suppression to the large stimuli while the other did not. In these two patterns, the contribution of the peak CCs became smaller when the grating stimulus was larger than the CRFs. And third, both cells did not significantly reduce activity to the grating patch larger than their CRFs. In this case, the peak contribution in CCs did not vary with an increase of the stimulus size. We concluded that the strength of firing interaction is positively correlated with the change in firing rate of cell pairs because of the change of stimulus sizes. We also analyzed CCs in respect of orientation preference of cell pairs. Although the significant peak CCs were most often observed for the common and optimal orientation of the cell pairs, there were some pairs that showed strong peaks for the nonpreferred orientation (more than 60° apart from the optimal) of stimulus, which evoked responses with low firing levels. This result suggests that the strength of firing correlation of cell pairs does not simply depend on the firing rate when the stimulus orientation is varied.

Contrast-Dependent Gain Control of the Contextual Response Modulation in the Cat Primary Visual Cortex

Neurons of the primary visual cortex (V1) respond to stimuli presented at the classical receptive field (CRF), and the responses are suppressively modulated by stimuli simultaneously presented at the receptive field surround (SRF) [1, 2]. The response modulation by an SRF stimulus depends on the stimulus orientation and spatial frequency; thus, it was suggested that intracortical mechanisms contribute to this phenomenon [2]. We recently reported that this suppressive modulation is not due to a direct inhibition to the cell by the intracortical inhibition [3] (also see the chapter by H. Ozeki et al., this volume).

Contribution of Excitation and Inhibition to the Stimulus Size- and Orientation-Tuning of Response Modulation by the Receptive Field Surround in the Cat Primary Visual Cortex

The response of neurons in the primary visual cortex (V1) is modulated by the stimulus presented at the surround of the classical receptive field (CRF), and the predominant effect of this surround stimulation is suppressive [1–5]. The strength of the surround suppression is dependent on the relationship of stimulus parameters, such as orientation and spatial frequency, between grating stimuli at the inside and outside of the CRF [1, 2]. Although properties of the surround suppression have been well characterized, input mechanisms underlying the stimulus-context-dependent response modulation and the size-tuning properties of V1 neurons have not been clarified yet. There is evidence that the surround suppression in VI is both sub-cortical [5] and intracortical [2, 4] in origin.

1809 Neuronal connectivity among barrels in the rat barrel cortex

TAKEHIKO ICHIKAWA’, TAKAFUMI AKASAKI’, SATOSHI SHIMEGI’, YUMIKO YOSHIMURA2, HIROMICHI SATO’ In the rat barrel cortex? the barrel columns are supposed to be functional modules for the vibrissal sensory information processing. To clarify the structure underlying the integration of information from multiple vibrissae, projection patterns in the barrel cortex were studied by a combination of neural staining with focal injections of a biotinylated dextran amine (BDA) and visualization of barrels and layers with cytochrome oxidase staining. Axonal projection from cells at the interbarrel region in layer IV (septa) avoided barrels but those in the supragranular and infragranular layers of the interbarrel region did not avoid barrel columns. Horizontal projections in both layers II/III and V were biased to the direction along the barrel row, however, the range of projection was more extensive in layer V than in layer II/III which often traversed three to four barrel columns. These connections could be the basis of the stimulus specific neural interactions in the barrel cortex.