Spiking Suppression Precedes Cued Attentional Enhancement of Neural Responses in Primary Visual Cortex

Abstract

Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naïve subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses.

Adaptation of Intracortical Signaling Concurs with Enhanced Encoding Efficiency

“…The initial current sink in V1 granular layers that occurs following onset of visual stimulation is indicative of retinogeniculate synaptic activation (Mitzdorf 1987; Schroeder et al 1998; Maier 2013; Godlove et al 2014; van Kerkoerle et al 2014). Subsequent current sinks in extragranular layers are believed to reflect net polarization due to subsequent, cortico-cortical processing (Douglas et al 1988; van Kerkoerle et al 2014; Cox et al 2017). We thus wanted to determine the relative magnitude of the repetition-related CSD response reduction for each of these laminar compartments (Fig.…”

“…This observation suggests that while intracortical processing plays a profound role for adaptation, the absence of intracortical activation underlies most repetition suppression in V1. In other words, repetition suppression in V1 does not seem to be caused by active inhibition from increased feedback from higher level areas, as heightened inhibition or increased feedback should be reflected in increased synaptic activation and thus a larger CSD response compared to the initial presentation of the stimulus (Spaak et al 2012; van Kerkoerle et al 2014; Cox et al 2017; van Kerkoerle et al 2017). Having said this, it should be noted that CSD alone cannot provide conclusive evidence regarding the precise synaptic mechanisms underlying repetition suppression since it represents a spatially summed population signal.…”

“…The resulting CSD from the formula above was multiplied by 0.4S/mm as an estimate of the electric conductivity of cortex (Logothetis et al 2007) to obtain current per unit volume. We eliminated channels at the top and the bottom of the electrode array that were void of any MUA visual response (see Cox et al 2017 for details). For display purposes, two-dimensional representations of CSD as a function of time and space were created by interpolating CSD between adjacent electrode contacts, followed by smoothing with a two-dimensional Gaussian filter ( s = 0.1mm and 15ms) (Pettersen et al 2006).…”

“…For display purposes, two-dimensional representations of CSD as a function of time and space were created by interpolating CSD between adjacent electrode contacts, followed by smoothing with a two-dimensional Gaussian filter ( s = 0.1mm and 15ms) (Pettersen et al 2006). Microelectrode contacts were determined to be located in the granular layer based on the initial sink of a flash-evoked CSD (see Maier et al 2010; Maier 2013; Dougherty et al 2015; Ninomiya et al 2015; Cox et al 2017 for details). Infragranular laminar compartment locations were determined by the position of the initial sink in response to a flashed stimulus and corroborated by additional neurophysiological criteria (Maier et al 2010), such as characteristic patterns of LFP power spectral density (van Kerkoerle et al 2014; Bastos et al 2018), signal correlations of the LFP between all channel combinations, and the latency (Self et al 2013) of stimulus-evoked MUA responses (Supplementary Fig.…”

“…We used a custom-designed mirror stereoscope (see Cox et al 2017) to evoke neuronal responses specific to each eye. For any given stimulus presentation, the stimulus could be presented to either the left eye, the right eye, or to both eyes simultaneously.…”