Silencing “Top-Down” Cortical Signals Affects Spike-Responses of Neurons in Cat’s “Intermediate” Visual Cortex

Abstract

We examined the effects of reversible inactivation of a higher-order, pattern/form-processing, postero-temporal visual (PTV) cortex on the background activities and spike-responses of single neurons in the ipsilateral cytoarchitectonic area 19 (putative area V3) of anesthetized domestic cats. Very occasionally (2/28), silencing recurrent “feedback” signals from PTV, resulted in significant and reversible reduction in background activity of area 19 neurons. By contrast, in large proportions of area 19 neurons, PTV inactivation resulted in: (i) significant reversible changes in the peak magnitude of their responses to visual stimuli (35.5%; 10/28); (ii) substantial reversible changes in direction selectivity indices (DSIs; 43%; 12/28); and (iii) reversible, upward shifts in preferred stimulus velocities (37%; 7/19). Substantial (≥20°) shifts in preferred orientation and/or substantial (≥20°) changes in width of orientation-tuning curves of area 19 neurons were however less common (26.5%; 4/15). In a series of experiments conducted earlier, inactivation of PTV also induced upward shifts in the preferred velocities of the ipsilateral cytoarchitectonic area 17 (V1) neurons responding optimally at low velocities. These upward shifts in preferred velocities of areas 19 and 17 neurons were often accompanied by substantial increases in DSIs. Thus, in both the primary visual cortex and the “intermediate” visual cortex (area 19), feedback from PTV plays a modulatory role in relation to stimulus velocity preferences and/or direction selectivity, that is, the properties which are usually believed to be determined by the inputs from the dorsal thalamus and/or feedforward inputs from the primary visual cortices. The apparent specialization of area 19 for processing information about stationary/slowly moving visual stimuli is at least partially determined, by the feedback from the higher-order pattern-processing visual area. Overall, the recurrent signals from the higher-order, pattern/form-processing visual cortex appear to play an important role in determining the magnitude of spike-responses and some “motion-related” receptive field properties of a substantial proportion of neurons in the intermediate form-processing visual area—area 19.

Characterization of Feedback Neurons in the High-Level Visual Cortical Areas That Project Directly to the Primary Visual Cortex in the Cat

“…Our statistical results showed that the higher-level visual cortical area 21a at the ventral stream of pathway and area PMLS at the dorsal stream had a comparable proportion of feedback neurons that back-projected directly to the V1 area, and the distribution of feedback neurons in these two higher-level visual areas was similar at cortical layer II–III, IV, V, and VI. These results suggest that the ventral and dorsal visual streams may closely interact through the V1 area during information processing, which is consistent with previous studies (Shen et al, 2006 ; Gilaie-Dotan et al, 2013 ; Zachariou et al, 2014 ; Huang et al, 2017 ; Mercier et al, 2017 ) and argues against the proposition of ventral vs. dorsal pathway segregation (Brown, 2009 ; Bracci and Op de Beeck, 2016 ; Milner, 2017 ). Further, this study also quantitatively compared the proportion of feedback neurons among different high-level visual cortical areas.…”

Effects of top-down influence suppression on behavioral and V1 neuronal contrast sensitivity functions in cats

“…How top-down influence affects visual perception at the behavioral level and neuronal processing in low-level visual areas is less well understood. Numerous physiological studies have shown that neuronal responses in the low-level visual areas can be altered when higher-order visual areas are affected by pharmacological administration ( Chen et al., 2014 ; Hishida et al., 2019 ; Tong et al., 2011 ; Yang et al., 2016b ), cooling ( Huang et al., 2017 ; Nassi et al., 2013 ; Wang et al., 2000 , 2007 , 2010 ), optogenetic manipulation ( Huh et al., 2018 ; Keller et al., 2020 ; Nurminen et al., 2018 ; Pafundo et al., 2016 ; Pak et al., 2020 ; Zhang et al., 2014 ), and attention ( Chalk et al., 2010 ; Lee and Maunsell, 2010 ; Li et al., 2008 ; Lu et al., 2011 ; Thiele et al., 2009 ; Williford and Maunsell, 2006 ), but the results are diverse or even contradictory ( Han and VanRullen, 2016 ; Harrison et al., 2007 ; Hishida et al., 2019 ; Huh et al., 2018 ; Lu et al., 2011 ; Murray et al., 2002 ; Nassi et al., 2013 ; Tong et al., 2011 ; Wang et al., 2000 , 2007 ; Zhang et al., 2014 ), probably because different modulation techniques might have caused variations in the time course and reversibility of top-down effects. Furthermore, these studies have not examined behavioral changes after acute modification of top-down influence ( Zhang et al., 2014 ).…”

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“…Our statistical results showed that the higher-level visual cortical area 21a at the ventral stream of pathway and area PMLS at the dorsal stream had a comparable proportion of feedback neurons that back-projected directly to the V1 area, and the distribution of feedback neurons in these two higher-level visual areas was similar at cortical layer II-III, IV, V, and VI. These results suggest that the ventral and dorsal visual streams may closely interact through the V1 area during information processing, which is consistent with previous studies (Shen et al, 2006;Gilaie-Dotan et al, 2013;Zachariou et al, 2014;Huang et al, 2017;Mercier et al, 2017) and argues against the proposition of ventral vs. dorsal pathway segregation (Brown, 2009;Bracci and Op de Beeck, 2016;Milner, 2017). Further, this study also quantitatively compared the proportion of feedback neurons among different high-level visual cortical areas.…”