Abstract
Throughout the brain, parallel processing streams compose the building blocks of complex neural functions. One of the most salient models for studying the functional specialization of parallel visual streams in the primate brain is the lateral geniculate nucleus (LGN) of the dorsal thalamus, through which the parvocellular and magnocellular channels, On-center and Off-center channels, and ipsilateral and contralateral eye channels are maintained and provide the foundation for cortical processing. We examined three aspects of neural processing in these streams: (1) the relationship between extraclassical surround suppression, a widespread visual computation thought to represent a canonical neural computation, and the parallel channels of the LGN; (2) the magnitude of binocular interaction in the parallel streams; and (3) the magnitude of suppression elicited by perceptual competition (binocular rivalry) in each stream. Our results show that surround suppression is almost exclusive to Off channel cells; further, we found evidence for two different components of monocular surround suppression—an early-stage suppression exhibited by all magnocellular cells, and a late-stage suppression exhibited only by Off cells in both the parvocellular and magnocellular pathways. This finding indicates that stream-specific circuits contribute to surround suppression in the primate LGN and suggests a distinct role for suppression in the Off channel to the cortex. We also examined the responses of LGN neurons in alert macaque monkeys to determine whether neurons that supply the cortex with visual information are influenced by stimulation of both eyes. Our results demonstrate that LGN neurons are not influenced by stimulation of the non-dominant eye. This was the case when dichoptic stimuli were presented to classical receptive fields of neurons, extraclassical receptive fields of neurons, and when stimuli were appropriate to produce the perception of binocular rivalry.
Highlights
Throughout the visual system, information is carried in parallel processing streams that contribute to functionally specific computations
Opportunities for stream mixing exist through local interneurons, thalamic reticular nucleus (TRN), and cortical feedback, which opens the interesting possibility that circuitry subserving inter-stream interactions, if present, could be differentiated based on the time course of the interactions
In our investigation of the stream-specificity of monocular surround suppression in the lateral geniculate nucleus (LGN), we found that surround suppression is carried predominantly by Off-channel cells, with magnocellular and parvocellular Off cells showing distinct temporal dynamics, indicating a functional specialization for these cells
Summary
Throughout the visual system, information is carried in parallel processing streams that contribute to functionally specific computations. For many neurons in the LGN, stimuli that extend beyond the classical receptive field of the neuron have a suppressive effect on the cells’ spiking activity (Hubel and Wiesel, 1961; Murphy and Sillito, 1987; Solomon et al, 2002; Bonin et al, 2005; Alitto and Usrey, 2008; Camp et al, 2009; Archer et al, 2021) This process is thought to represent a contrast-dependent gain control mechanism (Bonin et al, 2005), and recent evidence has suggested that there are stream-dependent differences in the magnitude of extraclassical suppression, with extraclassical suppression being stronger in the magnocellular stream than in the parvocellular stream (Solomon et al, 2002; Webb et al, 2002, 2005; Alitto and Usrey, 2008; Archer et al, 2021), and that within the magnocellular stream, extraclassical suppression is stronger in Off-cells than in On-cells (Archer et al, 2021). It remains unclear whether the temporal dynamics of suppression in these streams are similar, and whether such Off-On dichotomy exists within the parvocellular stream
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