Competitive Stimulus Interactions within Single Response Fields of Superior Colliculus Neurons

Department of Ophthalmology and Visual Sciences, University of Wisconsin–Madison, Madison, Wisconsin, United States
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 01/2006; 25(49):11357-73. DOI: 10.1523/JNEUROSCI.3825-05.2005
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In addition to its role in saccade generation, the superior colliculus (SC) is involved in target selection, saccade selection, and shifting the focus of spatial attention. Here, we investigated the influence of saccade selection on sensory interactions within single response fields (RFs) of SC neurons. One or two differently shaped stimuli were presented within single RFs of SC neurons, and the shape of a centrally located cue indicated whether and where to make a saccade (Go-Go) or whether to make or withhold a saccade (Go/No-Go). We found that, when two stimuli appeared at different locations within a single RF, SC neuronal activity was reduced compared with when a single stimulus appeared in isolation within the center of the RF in both the Go-Go and Go/No-Go tasks. In both tasks, a subsequent cue indicating one stimulus as a saccade target reduced the influence of the second stimulus located within the RF. We found that the time course of the suppression resulting from the two stimuli was approximately 130 ms, a time close to that seen in cortex. Finally, we found that the influence of two stimuli within single RFs of SC neurons changed over time in both the Go-Go and the Go/No-Go tasks. Initially, the neurons averaged the influence of two stimuli. As the trial progressed, the SC neurons signaled only the saccade vector that was produced. We conclude that cues to shift gaze, like attention, modulate the influence of sensory interactions, providing additional support for the linkage between attention and saccade selection.

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Available from: Xiaobing Li, Feb 20, 2014
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    • "Eleven sites were in monkey E, 17 were in monkey B, 24 were in monkey H, and 17 were in monkey L. At each site we first recorded neuronal activity to characterize it at that site. We observed response profiles of nigral neurons similar to those previously reported by us and others (Basso and Liu 2007; Basso and Wurtz 2002; Basso et al. 2005; Bayer et al. 2002; Handel and Glimcher 1999, 2000; Hikosaka and Wurtz 1983a, 1983b, 1983c; Liu and Basso 2008). After briefly documenting the local response properties, we introduced electrical stimulation at the site during performance of the memory-guided saccade task or the visually guided saccade task. "
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    ABSTRACT: In the absence of sensory information, we rely on past experience or memories to guide our actions. Previous reports implicate basal ganglia nuclei in the generation of movement in the absence of sensory stimuli. Here, we ask whether one output nucleus of the basal ganglia, the substantia nigra pars reticulata (nigra), influences eye movements in the absence of sensory information to guide the movement. We manipulated the level of activity of neurons in the nigra by introducing electrical stimulation to the nigra at different time intervals while monkeys made saccades to different locations in two conditions; one in which the target location remained visible and a second in which the target location appeared only briefly, requiring information stored in memory to specify the movement. Electrical manipulation of the nigra occurring during the delay-period of the task, when information about the target was maintained in memory, altered the direction and the occurrence of subsequent saccades. Stimulation during other intervals of the memory task or during the delay-period of the visually-guided saccade task had less effect on eye movements. Because these effects occurred with manipulation of nigral activity well before the initiation of saccades and in trials in which the visual stimulus was absent, we conclude that information from the basal ganglia influences the specification of an action as it is evolving primarily during performance of memory-guided saccades. When visual information is available to guide the specification of the saccade, as occurs during visually-guided saccades, basal ganglia information is less influential.
    Journal of Neurophysiology 11/2013; 111(4). DOI:10.1152/jn.00002.2013 · 2.89 Impact Factor
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    • "In the random-dot motion discrimination, for example, LIP neurons show a timeand coherence-dependent reduction in activity when evidence favors a saccade away from the RF (Roitman and Shadlen, 2002; Mazurek et al., 2003). Multiple stimuli within a RF lead to competitive interactions and a reduction in activity in superior colliculus neurons, which are strongly interconnected with LIP (Li and Basso, 2005), in a process akin to divisive normalization (Carandini and Heeger, 2011). Positive and negative profiles of graded responses are sufficient to support the basic characteristics of numerical judgments. "
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    ABSTRACT: Humans and animals appear to share a similar representation of number as an analog magnitude on an internal, subjective scale. Neurological and neurophysiological data suggest that posterior parietal cortex (PPC) is a critical component of the circuits that form the basis of numerical abilities in humans. Patients with parietal lesions are impaired in their ability to access the deep meaning of numbers. Acalculiac patients with inferior parietal damage often have difficulty performing arithmetic (2 + 4?) or number bisection (what is between 3 and 5?) tasks, but are able to recite multiplication tables and read or write numerals. Functional imaging studies of neurologically intact humans performing subtraction, number comparison, and non-verbal magnitude comparison tasks show activity in areas within the intraparietal sulcus (IPS). Taken together, clinical cases and imaging studies support a critical role for parietal cortex in the mental manipulation of numerical quantities. Further, responses of single PPC neurons in non-human primates are sensitive to the numerosity of visual stimuli independent of low-level stimulus qualities. When monkeys are trained to make explicit judgments about the numerical value of such stimuli, PPC neurons encode their cardinal numerical value; without such training PPC neurons appear to encode numerical magnitude in an analog fashion. Here we suggest that the spatial and integrative properties of PPC neurons contribute to their critical role in numerical cognition.
    Frontiers in Integrative Neuroscience 05/2012; 6:25. DOI:10.3389/fnint.2012.00025
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    • "The SC participates in guiding orientation behaviors by translating sensory signals into appropriate motor commands. Given a competitive stimulus environment, SC sensory maps can temporarily represent multiple conflicting targets that require resolution before an accurate motor command towards a selected target can be issued (Keller and McPeek 2002; Li and Basso 2005; McPeek and Keller 2002). Numerous prior studies have shown that multisensory integration of spatiotemporally concordant modality-specific cues leads to enhanced activity for individual SC neurons (Jiang et al. 2001; King and Palmer 1985; Meredith et al. 1987; Meredith and Stein 1996; Stein and Meredith 1993). "
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    ABSTRACT: In environments containing sensory events at competing locations, selecting a target for orienting requires prioritization of stimulus values. Although the superior colliculus (SC) is causally linked to the stimulus selection process, the manner in which SC multisensory integration operates in a competitive stimulus environment is unknown. Here we examined how the activity of visual-auditory SC neurons is affected by placement of a competing target in the opposite hemifield, a stimulus configuration that would, in principle, promote interhemispheric competition for access to downstream motor circuitry. Competitive interactions between the targets were evident in how they altered unisensory and multisensory responses of individual neurons. Responses elicited by a cross-modal stimulus (multisensory responses) proved to be substantially more resistant to competitor-induced depression than were unisensory responses (evoked by the component modality-specific stimuli). Similarly, when a cross-modal stimulus served as the competitor, it exerted considerably more depression than did its individual component stimuli, in some cases producing more depression than predicted by their linear sum. These findings suggest that multisensory integration can help resolve competition among multiple targets by enhancing orientation to the location of cross-modal events while simultaneously suppressing orientation to events at alternate locations.
    Journal of Neurophysiology 09/2011; 106(6):3091-101. DOI:10.1152/jn.00509.2011 · 2.89 Impact Factor
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