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

Abstract

Summary To explore the relative contributions of higher-order and primary visual cortex (V1) to visual perception, we compared cats' behavioral and V1 neuronal contrast sensitivity functions (CSF) and threshold versus external noise contrast (TvC) functions before and after top-down influence of area 7 (A7) was modulated with transcranial direct current stimulation (tDCS). We found that suppressing top-down influence of A7 with cathode-tDCS, but not sham-tDCS, reduced behavioral and neuronal contrast sensitivity in the same range of spatial frequencies and increased behavioral and neuronal contrast thresholds in the same range of external noise levels. The neuronal CSF and TvC functions were highly correlated with their behavioral counterparts both before and after the top-down suppression. Analysis of TvC functions using the Perceptual Template Model (PTM) indicated that top-down influence of A7 increased both behavioral and V1 neuronal contrast sensitivity by reducing internal additive noise and the impact of external noise.

Suppression of top-down influence decreases both behavioral and V1 neuronal response sensitivity to stimulus orientations in cats

“…Numerous studies have shown that transcranial direct current stimulation (tDCS) is a reliable non-invasive tool that can reversibly modulate neuronal excitability in the stimulated local brain region, with anode (a)-and cathode (c)-tDCS, respectively, enhancing and suppressing neuronal activity for a long-lasting (60-90 min) effect (Nitsche and Paulus, 2001;Schweid et al, 2008;Stagg et al, 2009;Monte-Silva et al, 2010;Bachtiar et al, 2015). Our recent investigations also demonstrate that c-and a-tDCS with the current intensity of 1 mA and a period of 15 min, respectively, decreases and enhances neuronal excitability with the effect confined in the stimulated cortical area and lasted for 60-70 min (Zhao et al, 2020;Ding et al, 2021Ding et al, , 2022. The current study will use tDCS tool to modulate top-down influence and observe concurrent change of both behavioral performance in orientation identification and the response selectivity of V1 neurons for stimulus orientations.…”

Mechanisms of Surround Suppression Effect on the Contrast Sensitivity of V1 Neurons in Cats

“…Furthermore, our recent studies show that suppression of top-down influence decreases the neuronal contrast sensitivity in the V1 cortex. This top-down suppression may be mediated by a stronger effect of internal noise elevation than of external noise admission at the perceptual template level [ 48 ], whereas it may occur through a larger effect in the reduction of response gain than of contrast gain on the contrast-response function of V1 neurons [ 32 ], and this top-down influence in response gain may relate to alterations in excitatory glutamatergic neurotransmission [ 103 – 105 ]. Finally, recent studies suggest that increased GABAergic inhibition may underlie noise filtering in the visual signal perception [ 106 , 107 ].…”

“…Equivalent internal noise can be estimated by comparison to the effects of external noise ( N ext ) added in the stimulus. By measuring the observer's performance in the detection of visual signals with different amounts of external noise, the PTM analysis can identify three pure mechanisms of (1) stimulus enhancement (equivalent to internal additive noise reduction), (2) external noise exclusion and (3) internal multiplicative noise suppression ( Figure 4 ), or a mixture of these mechanisms in attention [ 38 , 42 ], perceptual learning [ 44 – 46 , 58 ], top-down influence [ 48 ], and brain development [ 63 ]. To assess the relative contributions from each or combinations of the noise sources to SS effect on neuronal contrast sensitivity, three weighting coefficients A a , A f , and A m corresponding to the noise source N a , N ext , and N m , respectively, were added in the original PTM equation to fit neuronal TvC functions obtained with and without surround stimuli: where C τ represents threshold contrast at the d ′ performance level; N a , N ext , N m , β , and γ denote, respectively, the standard deviation of internal additive noise, the standard deviation of external noise, the proportional constant of multiplicative noise, the gain of the perceptual template, and the exponent of the nonlinear transducer.…”

“…The contrast of circular grating stimuli varied between 0% and 100%, and the contrast of annular grating stimuli was fixed at 100%. 4 Neural Plasticity suppression (Figure 4), or a mixture of these mechanisms in attention [38,42], perceptual learning [44][45][46]58], top-down influence [48], and brain development [63]. To assess the relative contributions from each or combinations of the noise sources to SS effect on neuronal contrast sensitivity, three weighting coefficients A a , A f , and A m corresponding to the noise source N a , N ext , and N m , respectively, were added in the original PTM equation to fit neuronal TvC functions obtained with and without surround stimuli:…”

“…Conversely, studies on perceptual contrast sensitivity functions are widely conducted at the system level to model observer performance in perceptual tasks using the perceptual template model (PTM) in terms of perceptual template(s), transducer nonlinearity, internal additive noise, and multiplicative noise [24,[38][39][40]. This PTM has been used to distinguish mechanisms of attention [41][42][43], perceptual learning [44][45][46][47], and top-down [48] effects on threshold contrast in the detection of visual signals. To identify the mechanisms of SS effects on neuronal contrast sensitivity at the system level, the present study applied the external noise paradigm and the PTM analysis to measure the SS effect on the contrast sensitivity of V1 neurons with different preferred SFs.…”