Synaptic Integration in Striate Cortical Simple Cells

Abstract

Simple cells in the visual cortex respond to the precise position of oriented contours (Hubel and Wiesel, 1962). This sensitivity reflects the structure of the simple receptive field, which exhibits two sorts of antagonism between on and off inputs. First, simple receptive fields are divided into adjacent on and off subregions; second, within each subregion, stimuli of the reverse contrast evoke responses of the opposite sign: push-pull (Hubel and Wiesel, 1962;Palmer and Davis, 1981;Jones and Palmer, 1987;Ferster, 1988). We have made whole-cell patch recordings from cat area 17 during visual stimulation to examine the generation and integration of excitation (push) and suppression (pull) in the simple receptive field. The temporal structure of the push reflected the pattern of thalamic inputs, as judged by comparing the intracellular cortical responses to extracellular recordings made in the lateral geniculate nucleus.Two mechanisms have been advanced to account for the pullwithdrawal of thalamic drive and active, intracortical inhibition (Hubel and Wiesel, 1962;Heggelund, 1986;Ferster, 1988). Our results suggest that intracortical inhibition is the dominant, and perhaps sole, mechanism of suppression. The inhibitory influences operated within a wide dynamic range. When inhibition was strong, the membrane conductance could be doubled or tripled. Furthermore, if a stimulus confined to one subregion was enlarged so that it extended into the next, the sign of response often changed from depolarizing to hyperpolarizing. In other instances, the inhibition modulated neuronal output subtly, by elevating spike threshold or altering firing rate at a given membrane voltage. Key words: visual cortex; patch recording in vivo; simple cell; IPSP; EPSP; spiny stellate cellCortical sensitivity to patterned stimuli has its roots in the arrangement of synaptic inputs to simple cells, whose receptive fields are made of elongated, alternating on and off subregions. Bright signals confined to an on subregion are excitatory, whereas dark ones reduce activity; that is, stimuli of the opposite contrast have a push -pull effect (Hubel and Wiesel, 1962;Movshon et al., 1978;Heggelund, 1981Heggelund, , 1986Palmer and Davis, 1981;Jones and Palmer, 1987;Ferster, 1988;Miller, 1994;Troyer et al., 1998; but see Debanne et al., 1998). Furthermore, when the receptive field is uniformly illuminated or darkened, simple cells respond poorly because their subregions have a mutually antagonistic relationship (Hubel and Wiesel, 1962). Thus, the output of the simple cell relies on the balance of excitation and suppression that various stimuli evoke.We have used the technique of whole-cell recording (Hamill et al., 1981;Edwards et al., 1989;Blanton et al., 1989) in vivo (Pei et al., 1991;Ferster and Jagadeesh, 1992) to analyze the synaptic mechanisms that produce visually evoked responses in the receptive field. First, we examined the origins of excitatory and suppressive components of the responses to stimuli of reverse contrast flashed within a single ...

A neuronal network model of macaque primary visual cortex (V1): Orientation selectivity and dynamics in the input layer 4Cα

“…This balance of currents immediately implies that the inhibitory conductance must be higher than the excitatory (g E V E Ӎ g I ͉V I ͉ f g I Ӎ (V E ͉͞V I ͉)g E ϭ 7g E ). The high (inhibitory) conductance regime at which the model operates is also supported by recent experiments: large inhibitory conductances, evoked by visual stimuli, have been observed experimentally in visual cortical cells (40,41).…”

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

“…It is also possible that the balance of excitation and inhibition plays an important role in regulating the tuning of spiking outputs of neurons near pinwheel centers. There is substantial evidence for shunting inhibition in V1 neurons [1,10,30,44], though the tuning of such inhibition is not entirely clear [1,44]. Shunting inhibition can effectively clamp the membrane potential, which has the effect of reducing the influence of excitatory synaptic inputs, and also reducing the variability of membrane potential [44].…”

Recruitment of Local Inhibitory Networks by Horizontal Connections in Layer 2/3 of Ferret Visual Cortex

“…Previous experiments have shown that single inhibitory cells elicit rather small changes in conductance and weak IPSPs (Ͻ1 mV in pyramidal cells depolarized by Յ20 mV; Gupta et al 2000;Thomson and Deuchars 1997). In contrast, in vivo intracellular recordings reveal much larger changes in inhibitory conductance during visual processing (Anderson et al 2000;BorgGraham et al 1998;Hirsch et al 1998). Taken together, these data indicate that inhibitory cells recruited by horizontal connections do not perform in isolation during cortical processing, but as part of coordinated inhibitory networks.…”