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Neural mechanisms of speed-accuracy tradeoff of visual search: saccade vigor, the origin of targeting errors, and comparison of the superior colliculus and frontal eye field.
Reppert TR, Servant M, Heitz RP, Schall JD
(2018) J Neurophysiol 120: 372-384
MeSH Terms: Animals, Decision Making, Macaca radiata, Psychomotor Performance, Saccades, Superior Colliculi, Visual Fields
Show Abstract · Added March 18, 2020
Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In "Accurate" relative to "Fast" trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. NEW & NOTEWORTHY Neurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This article reports the first replication of SAT performance in nonhuman primates, the first report of variation of saccade dynamics with SAT, the first description of superior colliculus contributions to SAT, and the first description of the origin of errors during SAT. These results inform and constrain new models of distributed decision making.
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MeSH Terms
Microsaccade production during saccade cancelation in a stop-signal task.
Godlove DC, Schall JD
(2016) Vision Res 118: 5-16
MeSH Terms: Animals, Attention, Fixation, Ocular, Humans, Inhibition, Psychological, Models, Theoretical, Neurons, Reaction Time, Saccades, Superior Colliculi, Visual Perception
Show Abstract · Added February 12, 2015
We obtained behavioral data to evaluate two alternative hypotheses about the neural mechanisms of gaze control. The "fixation" hypothesis states that neurons in rostral superior colliculus (SC) enforce fixation of gaze. The "microsaccade" hypothesis states that neurons in rostral SC encode microsaccades rather than fixation per se. Previously reported neuronal activity in monkey SC during the saccade stop-signal task leads to specific, dissociable behavioral predictions of these two hypotheses. When subjects are required to cancel partially-prepared saccades, imbalanced activity spreads across rostral and caudal SC with a reliable temporal profile. The microsaccade hypothesis predicts that this imbalance will lead to elevated microsaccade production biased toward the target location, while the fixation hypothesis predicts reduced microsaccade production. We tested these predictions by analyzing the microsaccades produced by 4 monkeys while they voluntarily canceled partially prepared eye movements in response to explicit stop signals. Consistent with the fixation hypothesis and contradicting the microsaccade hypothesis, we found that each subject produced significantly fewer microsaccades when normal saccades were successfully canceled. The few microsaccades escaping this inhibition tended to be directed toward the target location. We additionally investigated interactions between initiating microsaccades and inhibiting normal saccades. Reaction times were longer when microsaccades immediately preceded target presentation. However, pre-target microsaccade production did not affect stop-signal reaction time or alter the probability of canceling saccades following stop signals. These findings demonstrate that imbalanced activity within SC does not necessarily produce microsaccades and add to evidence that saccade preparation and cancelation are separate processes.
Copyright © 2014 Elsevier Ltd. All rights reserved.
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11 MeSH Terms
Multisensory response modulation in the superficial layers of the superior colliculus.
Ghose D, Maier A, Nidiffer A, Wallace MT
(2014) J Neurosci 34: 4332-44
MeSH Terms: Animals, Auditory Perception, Cats, Evoked Potentials, Auditory, Evoked Potentials, Visual, Male, Nerve Net, Neurons, Superior Colliculi, Visual Pathways, Visual Perception
Show Abstract · Added January 20, 2015
The mammalian superior colliculus (SC) is made up of seven distinct layers. Based on overall differences in neuronal morphology, afferent and efferent projection patterns, physiological properties, and presumptive behavioral role, the upper three layers have been classically grouped together as the superficial layers and the remaining four layers collectively make up the deep layers. Although the superficial layers receive their primary inputs from the retina and primary visual cortex, the deep layers receive inputs from extrastriate visual cortical areas and from auditory, somatosensory, and motor-related structures. In contrast, there is no evidence of monosynaptic nonvisual inputs to the superficial layers. However, more recent studies have revealed anatomical connections between the superficial and deep layers, thus providing the substrate for possible communication between these two functional divisions of the SC. In this study, we provide physiological evidence for auditory influences on visual responses in the superficial layers of the SC. Using extracellular recordings of local field potentials (LFPs) and multiunit activity, we demonstrate multisensory effects in the superficial layers of the cat SC such that subthreshold auditory activity (as seen in the LFP) modulates visual responses (reflected in spiking activity) when the two stimuli are presented together. These results have important implications for our understanding of the functional organization of the SC and for the neural basis of multisensory integration in general.
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11 MeSH Terms
Absence of transient receptor potential vanilloid-1 accelerates stress-induced axonopathy in the optic projection.
Ward NJ, Ho KW, Lambert WS, Weitlauf C, Calkins DJ
(2014) J Neurosci 34: 3161-70
MeSH Terms: Animals, Axons, Cholera Toxin, Disease Models, Animal, Functional Laterality, Intraocular Pressure, Male, Membrane Potentials, Mice, Mice, Inbred C57BL, Mice, Transgenic, Nerve Degeneration, Ocular Hypertension, Optic Nerve Diseases, Patch-Clamp Techniques, Rats, Retinal Ganglion Cells, Superior Colliculi, TRPV Cation Channels, Visual Pathways
Show Abstract · Added May 27, 2014
How neurons respond to stress in degenerative disease is of fundamental importance for identifying mechanisms of progression and new therapeutic targets. Members of the transient receptor potential (TRP) family of cation-selective ion channels are candidates for mediating stress signals, since different subunits transduce a variety of stimuli relevant in both normal and pathogenic physiology. We addressed this possibility for the TRP vanilloid-1 (TRPV1) subunit by comparing how the optic projection of Trpv1(-/-) mice and age-matched C57 controls responds to stress from elevated ocular pressure, the critical stressor in the most common optic neuropathy, glaucoma. Over a 5 week period of elevated pressure induced by microbead occlusion of ocular fluid, Trpv1(-/-) accelerated both degradation of axonal transport from retinal ganglion cells to the superior colliculus and degeneration of the axons themselves in the optic nerve. Ganglion cell body loss, which is normally later in progression, occurred in nasal sectors of Trpv1(-/-) but not C57 retina. Pharmacological antagonism of TRPV1 in rats similarly accelerated ganglion cell axonopathy. Elevated ocular pressure resulted in differences in spontaneous firing rate and action potential threshold current in Trpv1(-/-) ganglion cells compared with C57. In the absence of elevated pressure, ganglion cells in the two strains had similar firing patterns. Based on these data, we propose that TRPV1 may help neurons respond to disease-relevant stressors by enhancing activity necessary for axonal signaling.
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20 MeSH Terms
Heterogeneity in the spatial receptive field architecture of multisensory neurons of the superior colliculus and its effects on multisensory integration.
Ghose D, Wallace MT
(2014) Neuroscience 256: 147-62
MeSH Terms: Acoustic Stimulation, Action Potentials, Analysis of Variance, Animals, Attention, Auditory Perception, Brain Mapping, Cats, Neurons, Photic Stimulation, Space Perception, Superior Colliculi
Show Abstract · Added March 19, 2014
Multisensory integration has been widely studied in neurons of the mammalian superior colliculus (SC). This has led to the description of various determinants of multisensory integration, including those based on stimulus- and neuron-specific factors. The most widely characterized of these illustrate the importance of the spatial and temporal relationships of the paired stimuli as well as their relative effectiveness in eliciting a response in determining the final integrated output. Although these stimulus-specific factors have generally been considered in isolation (i.e., manipulating stimulus location while holding all other factors constant), they have an intrinsic interdependency that has yet to be fully elucidated. For example, changes in stimulus location will likely also impact both the temporal profile of response and the effectiveness of the stimulus. The importance of better describing this interdependency is further reinforced by the fact that SC neurons have large receptive fields, and that responses at different locations within these receptive fields are far from equivalent. To address these issues, the current study was designed to examine the interdependency between the stimulus factors of space and effectiveness in dictating the multisensory responses of SC neurons. The results show that neuronal responsiveness changes dramatically with changes in stimulus location - highlighting a marked heterogeneity in the spatial receptive fields of SC neurons. More importantly, this receptive field heterogeneity played a major role in the integrative product exhibited by stimulus pairings, such that pairings at weakly responsive locations of the receptive fields resulted in the largest multisensory interactions. Together these results provide greater insight into the interrelationship of the factors underlying multisensory integration in SC neurons, and may have important mechanistic implications for multisensory integration and the role it plays in shaping SC-mediated behaviors.
Copyright © 2013 IBRO. Published by Elsevier Ltd. All rights reserved.
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12 MeSH Terms
Failure of axonal transport induces a spatially coincident increase in astrocyte BDNF prior to synapse loss in a central target.
Crish SD, Dapper JD, MacNamee SE, Balaram P, Sidorova TN, Lambert WS, Calkins DJ
(2013) Neuroscience 229: 55-70
MeSH Terms: Animals, Astrocytes, Axonal Transport, Brain-Derived Neurotrophic Factor, Disease Models, Animal, Glaucoma, Mice, Optic Nerve Diseases, RNA, Messenger, Rats, Retinal Ganglion Cells, Superior Colliculi, Synapses, Visual Pathways
Show Abstract · Added May 27, 2014
Failure of anterograde transport to distal targets in the brain is a common feature of neurodegenerative diseases. We have demonstrated in rodent models of glaucoma, the most common optic neuropathy, early loss of anterograde transport along the retinal ganglion cell (RGC) projection to the superior colliculus (SC) is retinotopic and followed by a period of persistence of RGC axon terminals and synapses through unknown molecular pathways. Here we use the DBA/2J mouse model of hereditary glaucoma and an acute rat model to demonstrate that retinotopically focal transport deficits in the SC are accompanied by a spatially coincident increase in brain-derived neurotrophic factor (BDNF), especially in hypertrophic astrocytes. These neurochemical changes occur prior to loss of RGC synapses in the DBA/2J SC. In contrast to BDNF protein, levels of Bdnf mRNA decreased with transport failure, even as mRNA encoding synaptic structures remained unchanged. In situ hybridization signal for Bdnf mRNA was the strongest in SC neurons, and labeling for the immature precursor pro-BDNF was very limited. Subcellular fractionation of SC indicated that membrane-bound BDNF decreased with age in the DBA/2J, while BDNF released from vesicles remained high. These results suggest that in response to diminished axonal function, activated astrocytes in the brain may sequester mature BDNF released from target neurons to counter stressors that otherwise would challenge survival of projection synapses.
Copyright © 2012 IBRO. Published by Elsevier Ltd. All rights reserved.
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1 Members
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14 MeSH Terms
Impact of response duration on multisensory integration.
Ghose D, Barnett ZP, Wallace MT
(2012) J Neurophysiol 108: 2534-44
MeSH Terms: Acoustic Stimulation, Animals, Cats, Evoked Potentials, Auditory, Evoked Potentials, Visual, Neurons, Afferent, Photic Stimulation, Superior Colliculi, Time
Show Abstract · Added March 19, 2014
Multisensory neurons in the superior colliculus (SC) have been shown to have large receptive fields that are heterogeneous in nature. These neurons have the capacity to integrate their different sensory inputs, a process that has been shown to depend on the physical characteristics of the stimuli that are combined (i.e., spatial and temporal relationship and relative effectiveness). Recent work has highlighted the interdependence of these factors in driving multisensory integration, adding a layer of complexity to our understanding of multisensory processes. In the present study our goal was to add to this understanding by characterizing how stimulus location impacts the temporal dynamics of multisensory responses in cat SC neurons. The results illustrate that locations within the spatial receptive fields (SRFs) of these neurons can be divided into those showing short-duration responses and long-duration response profiles. Most importantly, discharge duration appears to be a good determinant of multisensory integration, such that short-duration responses are typically associated with a high magnitude of multisensory integration (i.e., superadditive responses) while long-duration responses are typically associated with low integrative capacity. These results further reinforce the complexity of the integrative features of SC neurons and show that the large SRFs of these neurons are characterized by vastly differing temporal dynamics, dynamics that strongly shape the integrative capacity of these neurons.
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9 MeSH Terms
Using high-resolution MR imaging at 7T to evaluate the anatomy of the midbrain dopaminergic system.
Eapen M, Zald DH, Gatenby JC, Ding Z, Gore JC
(2011) AJNR Am J Neuroradiol 32: 688-94
MeSH Terms: Adult, Algorithms, Brain Mapping, Dopamine, Female, Humans, Magnetic Resonance Imaging, Male, Mesencephalon, Red Nucleus, Reference Values, Substantia Nigra, Superior Colliculi, Young Adult
Show Abstract · Added March 7, 2014
BACKGROUND AND PURPOSE - Dysfunction of DA neurotransmission from the SN and VTA has been implicated in neuropsychiatric diseases, including Parkinson disease and schizophrenia. Unfortunately, these midbrain DA structures are difficult to define on clinical MR imaging. To more precisely evaluate the anatomic architecture of the DA midbrain, we scanned healthy participants with a 7T MR imaging system. Here we contrast the performance of high-resolution T2- and T2*-weighted GRASE and FFE MR imaging scans at 7T.
MATERIALS AND METHODS - Ten healthy participants were scanned by using GRASE and FFE sequences. CNRs were calculated among the SN, VTA, and RN, and their volumes were estimated by using a segmentation algorithm.
RESULTS - Both GRASE and FFE scans revealed visible contrast between midbrain DA regions. The GRASE scan showed higher CNRs compared with the FFE scan. The T2* contrast of the FFE scan further delineated substructures and microvasculature within the midbrain SN and RN. Segmentation and volume estimation of the midbrain SN, RN, and VTA showed individual differences in the size and volume of these structures across participants.
CONCLUSIONS - Both GRASE and FFE provide sufficient CNR to evaluate the anatomy of the midbrain DA system. The FFE in particular reveals vascular details and substructure information within the midbrain regions that could be useful for examining structural changes in midbrain pathologies.
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2 Members
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14 MeSH Terms
Spatial receptive field organization of multisensory neurons and its impact on multisensory interactions.
Krueger J, Royal DW, Fister MC, Wallace MT
(2009) Hear Res 258: 47-54
MeSH Terms: Animals, Auditory Perception, Cats, Cerebral Cortex, Hearing, Models, Biological, Models, Neurological, Neurons, Sensation, Sensory Thresholds, Space Perception, Superior Colliculi, Time Factors, Vision, Ocular, Visual Perception
Show Abstract · Added March 19, 2014
Previous work has established that the spatial receptive fields (SRFs) of multisensory neurons in the cerebral cortex are strikingly heterogeneous, and that SRF architecture plays an important deterministic role in sensory responsiveness and multisensory integrative capacities. The initial part of this contribution serves to review these findings detailing the key features of SRF organization in cortical multisensory populations by highlighting work from the cat anterior ectosylvian sulcus (AES). In addition, we have recently conducted parallel studies designed to examine SRF architecture in the classic model for multisensory studies, the cat superior colliculus (SC), and we present some of the preliminary observations from the SC here. An examination of individual SC neurons revealed marked similarities between their unisensory (i.e., visual and auditory) SRFs, as well as between these unisensory SRFs and the multisensory SRF. Despite these similarities within individual neurons, different SC neurons had SRFs that ranged from a single area of greatest activation (hot spot) to multiple and spatially discrete hot spots. Similar to cortical multisensory neurons, the interactive profile of SC neurons was correlated strongly to SRF architecture, closely following the principle of inverse effectiveness. Thus, large and often superadditive multisensory response enhancements were typically seen at SRF locations where visual and auditory stimuli were weakly effective. Conversely, subadditive interactions were seen at SRF locations where stimuli were highly effective. Despite the unique functions characteristic of cortical and subcortical multisensory circuits, our results suggest a strong mechanistic interrelationship between SRF microarchitecture and integrative capacity.
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15 MeSH Terms
Development and plasticity of intra- and intersensory information processing.
Polley DB, Hillock AR, Spankovich C, Popescu MV, Royal DW, Wallace MT
(2008) J Am Acad Audiol 19: 780-98
MeSH Terms: Animals, Auditory Cortex, Auditory Pathways, Auditory Perception, Brain Mapping, Hearing, Humans, Neuronal Plasticity, Research Design, Superior Colliculi, Visual Pathways, Visual Perception
Show Abstract · Added March 19, 2014
The functional architecture of sensory brain regions reflects an ingenious biological solution to the competing demands of a continually changing sensory environment. While they are malleable, they have the constancy necessary to support a stable sensory percept. How does the functional organization of sensory brain regions contend with these antithetical demands? Here we describe the functional organization of auditory and multisensory (i.e., auditory-visual) information processing in three sensory brain structures: (1) a low-level unisensory cortical region, the primary auditory cortex (A1); (2) a higher-order multisensory cortical region, the anterior ectosylvian sulcus (AES); and (3) a multisensory subcortical structure, the superior colliculus (SC). We then present a body of work that characterizes the ontogenic expression of experience-dependent influences on the operations performed by the functional circuits contained within these regions. We will present data to support the hypothesis that the competing demands for plasticity and stability are addressed through a developmental transition in operational properties of functional circuits from an initially labile mode in the early stages of postnatal development to a more stable mode in the mature brain that retains the capacity for plasticity under specific experiential conditions. Finally, we discuss parallels between the central tenets of functional organization and plasticity of sensory brain structures drawn from animal studies and a growing literature on human brain plasticity and the potential applicability of these principles to the audiology clinic.
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12 MeSH Terms