Spatiotemporal flow of information in the early visual pathway

Abstract

The spatial components of a visual scene are processed neurally in a sequence of coarse features followed by fine features. This coarse-to-fine temporal stream was initially considered to be a cortical function, but has recently been demonstrated in the dorsal lateral geniculate nucleus. The goal of this study was to test the hypothesis that coarse-to-fine processing is present at earlier stages of visual processing in the retinal ganglion cells that supply lateral geniculate nucleus (LGN) neurons. To compare coarse-to-fine processing in the cat’s visual system, we measured the visual responses of connected neuronal pairs from the retina and LGN, and separate populations of cells from each region. We found that coarse-to-fine processing was clearly present at the ganglion cell layer of the retina. Interestingly, peak and high-spatial-frequency cutoff responses were higher in the LGN than in the retina, indicating that there was a progressive cascade of coarse-to-fine information from the retina to the LGN to the visual cortex. The analysis of early visual pathway receptive field characteristics showed that the physiological response interplay between the center and surround regions was consistent with coarse-to-fine features and may provide a primary role in the underlying mechanism. Taken together, the results from this study provided a framework for understanding the emergence and refinement of coarse-to-fine processing in the visual system.

Retinal and Nonretinal Contributions to Extraclassical Surround Suppression in the Lateral Geniculate Nucleus

“…In support of this possibility, an examination of contrast response functions generated from LGN neurons in alert and anesthetized animals indicates that anesthesia acts to scale neuronal firing rate in a divisive fashion over a wide range of contrasts (Alitto et al, 2011). Likewise, spatial attention has been shown to augment LGN responses, presumably by decreasing inhibition from the TRN (McAlonan et al, 2006(McAlonan et al, , 2008. Because thalamic inhibition is modulated by the brainstem, basal forebrain, and numerous cortical areas, extraclassical suppression may be a dynamic property of LGN neurons that can be modulated differentially by behavior and behavioral state to gate the thalamocortical transmission of retinal information to cortex.…”

“…Surround suppression in the retina not only decreases retinal firing rate, but also shifts the distribution of interspike intervals (ISIs) toward longer values. Because past work has shown that retinal spikes after longer ISIs are less effective in evoking a geniculate response (Mastronarde, 1987;Usrey et al, 1998;Levine and Cleland, 2001;Sincich et al, 2007;Weyand, 2007;Rathbun et al, 2010), an ISIdependent mechanism can augment suppression between the retina and LGN (Alitto and Usrey, 2015a). To estimate the contribution of retinal ISI to LGN surround suppression in the current study, we generated ISI efficacy functions for each retinogeniculate cell pair (Usrey et al, 1998).…”

“…However, given the relatively long visual response latencies of V1 neurons compared with LGN neurons along with the time required for action potentials to propagate from the cortex to the LGN and the added time needed to engage polysynaptic circuits for inhibition within the thalamus (Harvey, 1978;Tsumoto and Suda, 1980;Hirsch et al, 1998;Usrey et al, 1999;Alonso et al, 2001;Briggs andUsrey, 2005, 2009;Liang et al, 2008), it seems unlikely that corticogeniculate feedback has much of an influence on the early phase of extraclassical suppression in the LGN. With this in mind, feedback could certainly contribute to later phases of suppression.…”

Spatiotemporal profiles of receptive fields of neurons in the lateral posterior nucleus of the cat LP-pulvinar complex

“…According to the coarse-to-fine processing model (Einevoll et al 2011;Moore et al 2014), early neuronal activity conveys coarse visual information, whereas late activity, through RF component interactions, carries more detailed information. Hence, following this model, LPm and LPl neurons would preferentially be associated to the processing taking place along the "what" and "where" pathways, respectively (Lomber 2001;Lomber et al 1996).…”

Visual Functions of the Thalamus

“…Originally reported by Hubel & Wiesel (1961), the stronger classical surrounds of LGN receptive fields are believed to play an important role in shifting the spatial frequency response functions of LGN neurons toward higher frequencies (Moore et al 2014). Moreover, because the onset of responses in the classical surround is delayed relative to the onset of responses in the center, there is a temporal cascade in coarse- to fine-tuning for preferred spatial frequencies between the retina and LGN (Moore et al 2014). Cellular mechanisms underlying the increased classical surround likely include feedforward disynaptic inhibition via LGN interneurons.…”