A sensory memory to preserve visual representations across eye movements

Abstract

Saccadic eye movements (saccades) disrupt the continuous flow of visual information, yet our perception of the visual world remains uninterrupted. Here we assess the representation of the visual scene across saccades from single-trial spike trains of extrastriate visual areas, using a combined electrophysiology and statistical modeling approach. Using a model-based decoder we generate a high temporal resolution readout of visual information, and identify the specific changes in neurons’ spatiotemporal sensitivity that underly an integrated perisaccadic representation of visual space. Our results show that by maintaining a memory of the visual scene, extrastriate neurons produce an uninterrupted representation of the visual world. Extrastriate neurons exhibit a late response enhancement close to the time of saccade onset, which preserves the latest pre-saccadic information until the post-saccadic flow of retinal information resumes. These results show how our brain exploits available information to maintain a representation of the scene while visual inputs are disrupted.

Neural correlates of perisaccadic visual mislocalization in extrastriate cortex

“…The classical GLM has been widely used for encoding and decoding neural responses in low-level visual areas (such as the retina, LGN, and V1) 62,63 , but they fall short in capturing the time-varying characteristics of higher-level visual areas. To model responses in these areas, nonstationary model frameworks that enables a time-varying extension of a GLM have been developed, which showed success in characterizing the perisaccadic spatiotemporal changes of neural response and reading out perisaccadic stimulus information on the same timescale of saccadic eye movements 42,49,64,65 . In the present study, we took advantage of this GLM framework (SVGLM) and developed a procedure to measure spatial bias based on instantaneous neural sensitivity at various locations to identify the neural components contributing to spatial bias.…”

“…By quantifying the statistical dependencies of spiking responses on several behavioral (e.g., eye movement) or external (e.g., visual stimuli) variables, however, point process statistical models provide a powerful means to capture the encoding and decoding of visual information as continuously varying with eye movements, with no assumption on the function of neurons. To investigate the neural basis of perisaccadic mislocalization, this study used a time-varying generalized linear model framework capable of capturing the fast spatiotemporal dynamics of neural sensitivity around the time of saccades 42,49 , and examine the link between perisaccadic visual responses and visuospatial perception.…”

Time-varying generalized linear models: characterizing and decoding neuronal dynamics in higher visual areas

“…Each approach mentioned above has its own pros and cons, but few of them can succeed in capturing the responses of neurons in the higher visual areas where multiplexed neural signals reflecting the interaction of sensory and non-sensory variables complicate the neural code ( Table 1 ). One such example is saccadic eye movements, which involve fast and complex modulations in neuronal sensitivity in the extrastriate visual areas and prefrontal cortex during the perisaccadic period ( Nakamura and Colby, 2002 ; Sommer and Wurtz, 2006 ; Zirnsak et al, 2011 , 2014 ; Neupane et al, 2016 , 2020 ; Niknam et al, 2019 ; Akbarian et al, 2021 ). Quantitatively characterizing the perisaccadic sensitivity modulations on the fast timescale of saccades is critical for understanding the neural basis of various perisaccadic perceptual phenomena.…”

“…Saccade experiments and saccade-related visual behavior stand as a potent and classical paradigm in visual neuroscience, serving as a robust tool to establish links between neural responses and behavior or cognition ( Honda, 1989 ; Nakamura and Colby, 2002 ; Awater and Lappe, 2004 ; Jeffries et al, 2007 ; Zirnsak et al, 2011 ; Irwin and Robinson, 2015 ; Wurtz, 2018 ). Saccade paradigms have been implemented to unravel the intricate physiological and circuit mechanisms underlying various cognitive processes, including visual perception, attention, memory, and more ( Deubel and Schneider, 1996 ; Ross et al, 1997 ; Friston et al, 2012 ; Cronin and Irwin, 2018 ; Edwards et al, 2018 ; Akbarian et al, 2021 ).…”

Widespread Receptive Field Remapping in Early Visual Cortex

“…Furthermore, while work in human psychophysics has confirmed that remapping preserves some 17,23 but perhaps not all 24 visual feature selectivity at the level of perception, whether feature selectivity is preserved in individual neurons as they remap remains an open question. Indeed, despite extensive study, much remains unknown about the properties and extent of receptive field remapping, in large part due to limitations of the spatiotemporal resolution at which the phenomenon was studied [25][26][27][28] .…”