Attention Selectively Gates Afferent Signal Transmission to Area V4

Abstract

Selective attention allows focusing on only part of the incoming sensory information. Neurons in the extrastriate visual cortex reflect such selective processing when different stimuli are simultaneously present in their large receptive fields. Their spiking response then resembles the response to the attended stimulus when presented in isolation. Unclear is where in the neuronal pathway attention intervenes to achieve such selective signal routing and processing. To investigate this question, we tagged two equivalent visual stimuli by independent broadband luminance noise and used the spectral coherence of these behaviorally irrelevant signals with the field potential of a local neuronal population in male macaque monkeys' area V4 as a measure for their respective causal influences. This new experimental paradigm revealed that signal transmission was considerably weaker for the not-attended stimulus. Furthermore, our results show that attention does not need to modulate responses in the input populations sending signals to V4 to selectively represent a stimulus, nor do they suggest a change of the V4 neurons' output gain depending on their feature similarity with the stimuli. Our results rather imply that selective attention uses a gating mechanism comprising the synaptic "inputs" that transmit signals from upstream areas into the V4 neurons. A minimal model implementing attention-dependent routing by gamma-band synchrony replicated the attentional gating effect and the signals' spectral transfer characteristics. It supports the proposal that selective interareal gamma-band synchrony subserves signal routing and explains our experimental finding that attention selectively gates signals already at the level of afferent synaptic input. Depending on the behavioral context, the brain needs to channel the flow of information through its networks of massively interconnected neurons. We designed an experiment that allows to causally assess routing of information originating from an attended object. We found that attention "gates" signals at the interplay between afferent fibers and the local neurons. A minimal model demonstrated that coherent gamma-rhythmic activity (∼60 Hz) between local neurons and their afferent-providing input neurons can realize the gating. Importantly, the attended signals did not need to be amplified already in an earlier processing stage, nor did they get amplified by a simple output response modulation. The method provides a useful tool to study mechanisms of dynamic network configuration underlying cognitive processes.

Serial dependence in numerosity perception

“…Again, the effect appears to be spatially specific for the position of the inducer stimulus (i.e., it does not extend to the probe stimulus presented in the opposite hemifield, which would have canceled out any effect), thus supporting the results from Experiment 2. Such a spatially specific effect triggered by attention appears to be consistent with a spatially specific attentional modulation (Somers, Dale, Seiffert, & Tootell, 1999 ; Grothe et al, 2018 ), whereby attention modulates specific regions of topographically organized early visual cortex corresponding to specific positions in the visual field. Intriguingly, these results may also suggest that the spatial specificity of the effect is directly determined (and modulated) by attention.…”

Signal transfer of visual stimuli to V4 occurs in gamma-rhythmic, pulsed information packages

“…Data from two adult male rhesus monkeys (Macaca mulatta) were used for this study. Parts of the data have been used in a previous publication (Grothe et al, 2018).…”

“…For positioning stimuli, receptive fields were mapped manually while the monkey was fixating centrally, followed by an automated mapping procedure consisting of rapid presentations of circular dots. Stimuli were placed at equal eccentricity in the RF such that they induced similarly strong gamma-rhythmic activity (for details see Grothe et al, 2018). This requirement was successfully fulfilled in 16 recording sessions, resulting in 35 recording sites in total (Monkey F: 23 sites, Monkey B: 12 sites).…”

“…Once is calculated, we compute the pooled value ̅̅̅̅ over a region of interest in frequency-time lag space to reduce a two-dimensional result to a single value. The region of interest was defined as a frequency-dependent cone of width ± , where = 1/ and denotes the onset delay of the neural response in V4 after stimulus onset which was 50ms in monkey F and 60ms in monkey B (see Grothe et al, 2018). We first took the average across lags within the frequency-dependent region of interest, and then took the mean of the time averages from 5 up to 15 Hz.…”

“…In consequence, effective connectivity can be modulated by establishing the appropriate phase relationship between the rhythmic activities of the presynaptic (sending) and post-synaptic (receiving) populations. This mechanism is in general being referred to as communication-through-coherence (CTC) (Fries, 2015(Fries, , 2005, or as routing-by-synchrony (RBS) (Grothe et al, 2018(Grothe et al, , 2012Kreiter, 2006;Palmigiano et al, 2017). Two studies demonstrating such a dynamic routing mechanism showed that V4 populations do indeed establish a stronger phase coherence with the presynaptic populations processing the attended stimulus than those processing the non-attended stimuli (Bosman et al, 2012;Grothe et al, 2012).…”