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Temporal dynamics of binocular integration in primary visual cortex.
Cox MA, Dougherty K, Westerberg JA, Schall MS, Maier A
(2019) J Vis 19: 13
MeSH Terms: Animals, Behavior, Animal, Female, Macaca radiata, Male, Neurons, Neurophysiology, Ocular Physiological Phenomena, Photic Stimulation, Reproducibility of Results, Time Factors, Vision, Binocular, Visual Cortex
Show Abstract · Added August 27, 2020
Whenever we open our eyes, our brain quickly integrates the two eyes' perspectives into a combined view. This process of binocular integration happens so rapidly that even incompatible stimuli are briefly fused before one eye's view is suppressed in favor of the other (binocular rivalry). The neuronal basis for this brief period of fusion during incompatible binocular stimulation is unclear. Neuroanatomically, the eyes provide two largely separate streams of information that are integrated into a binocular response by the primary visual cortex (V1). However, the temporal dynamics underlying the formation of this binocular response are largely unknown. To address this question, we examined the temporal profile of binocular responses in V1 of fixating monkeys. We found that V1 processes binocular stimuli in a dynamic sequence that comprises at least two distinct temporal phases. An initial transient phase is characterized by enhanced spiking responses for both compatible and incompatible binocular stimuli compared to monocular stimulation. This transient is followed by a sustained response that differed markedly between congruent and incongruent binocular stimulation. Specifically, incompatible binocular stimulation resulted in overall response reduction relative to monocular stimulation (binocular suppression). In contrast, responses to compatible stimuli were either suppressed or enhanced (binocular facilitation) depending on the neurons' ocularity (selectivity for one eye over the other) and laminar location. These results suggest that binocular integration in V1 occurs in at least two sequential steps that comprise initial additive combination of the two eyes' signals followed by widespread differentiation between binocular concordance and discordance.
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Disrupted Habituation in the Early Stage of Psychosis.
Avery SN, McHugo M, Armstrong K, Blackford JU, Woodward ND, Heckers S
(2019) Biol Psychiatry Cogn Neurosci Neuroimaging 4: 1004-1012
MeSH Terms: Adult, Female, Habituation, Psychophysiologic, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Memory Disorders, Pattern Recognition, Visual, Psychotic Disorders, Schizophrenia, Visual Cortex, Young Adult
Show Abstract · Added January 31, 2020
BACKGROUND - Learning and memory are impaired in schizophrenia. Some theories have proposed that one form of memory, habituation, is particularly impaired. Preliminary evidence suggests that memory impairment is associated with failed hippocampal habituation in patients with chronic schizophrenia. We studied how abnormal habituation of the hippocampus is related to relational memory deficits in the early stage of psychosis.
METHODS - We measured hippocampal activity in 62 patients with early psychosis and 70 healthy individuals using functional magnetic resonance imaging. Habituation was defined as the slope of functional magnetic resonance imaging signal change to repeated presentations of faces and objects. Relational memory ability was measured as the slope of preferential viewing during a face-scene pair eye movement task outside the scanner.
RESULTS - Patients with early psychosis showed impaired relational memory (p < .001) and less hippocampal habituation to objects (p = .01) than healthy control subjects. In the healthy control group, better relational memory was associated with faster anterior hippocampal habituation (faces, r = -.28, p = .03). In contrast, patients with early psychosis showed no brain-behavior relationship (r = .12, p = .40).
CONCLUSIONS - We found evidence for disrupted hippocampal habituation in the early stage of psychosis along with an altered association between hippocampal habituation and relational memory ability. These results suggest that neural habituation may provide a novel target for early cognitive interventions in psychosis.
Copyright © 2019 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
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13 MeSH Terms
Figure-Ground Modulation in the Human Lateral Geniculate Nucleus Is Distinguishable from Top-Down Attention.
Poltoratski S, Maier A, Newton AT, Tong F
(2019) Curr Biol 29: 2051-2057.e3
MeSH Terms: Adult, Female, Geniculate Bodies, Humans, Magnetic Resonance Imaging, Male, Photic Stimulation, Visual Cortex, Visual Pathways, Young Adult
Show Abstract · Added August 27, 2020
Nearly all of the information that reaches the primary visual cortex (V1) of the brain passes from the retina through the lateral geniculate nucleus (LGN) of the thalamus. Although the LGN's role in relaying feedforward signals from the retina to the cortex is well understood [1, 2], the functional role of the extensive feedback it receives from the cortex has remained elusive [3-6]. Here, we investigated whether corticothalamic feedback may contribute to perceptual processing in the LGN in a manner that is distinct from top-down effects of attention [7-10]. We used high-resolution fMRI at 7 Tesla to simultaneously measure responses to orientation-defined figures in the human LGN and V1. We found robust enhancement of perceptual figures throughout the early visual system, which could be distinguished from the effects of covert spatial attention [11-13]. In a second experiment, we demonstrated that figure enhancement occurred in the LGN even when the figure and surrounding background were presented dichoptically (i.e., to different eyes). As binocular integration primarily occurs in V1 [14, 15], these results implicate a mechanism of automatic, contextually sensitive feedback from binocular visual cortex underlying figure-ground modulation in the LGN. Our findings elucidate the functional mechanisms of this core function of the visual system [16-18], which allows people to segment and detect meaningful figures in complex visual environments. The involvement of the LGN in this rich, contextually informed visual processing-despite showing minimal feedforward selectivity for visual features [19, 20]-underscores the role of recurrent processing at the earliest stages of visual processing.
Copyright © 2019 Elsevier Ltd. All rights reserved.
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V1 microcircuit dynamics: altered signal propagation suggests intracortical origins for adaptation in response to visual repetition.
Westerberg JA, Cox MA, Dougherty K, Maier A
(2019) J Neurophysiol 121: 1938-1952
MeSH Terms: Adaptation, Physiological, Animals, Evoked Potentials, Visual, Female, Geniculate Bodies, Macaca radiata, Male, Neurons, Visual Cortex
Show Abstract · Added August 27, 2020
Repetitive visual stimulation profoundly changes sensory processing in the primary visual cortex (V1). We show how the associated adaptive changes are linked to an altered flow of synaptic activation across the V1 laminar microcircuit. Using repeated visual stimulation, we recorded layer-specific responses in V1 of two fixating monkeys. We found that repetition-related spiking suppression was most pronounced outside granular V1 layers that receive the main retinogeniculate input. This repetition-related response suppression was robust to alternating stimuli between the eyes, in line with the notion that repetition-related adaptation is predominantly of cortical origin. Most importantly, current source density (CSD) analysis, which provides an estimate of local net depolarization, revealed that synaptic processing during repeated stimulation was most profoundly affected within supragranular layers, which harbor the bulk of cortico-cortical connections. Direct comparison of the temporal evolution of laminar CSD and spiking activity showed that stimulus repetition first affected supragranular synaptic currents, which translated into a reduction of stimulus-evoked spiking across layers. Together, these results suggest that repetition induces an altered state of intracortical processing that underpins visual adaptation. Our survival depends on our brains rapidly adapting to ever changing environments. A well-studied form of adaptation occurs whenever we encounter the same or similar stimuli repeatedly. We show that this repetition-related adaptation is supported by systematic changes in the flow of sensory activation across the laminar cortical microcircuitry of primary visual cortex. These results demonstrate how adaptation impacts neuronal interactions across cortical circuits.
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Binocular Modulation of Monocular V1 Neurons.
Dougherty K, Cox MA, Westerberg JA, Maier A
(2019) Curr Biol 29: 381-391.e4
MeSH Terms: Animals, Female, Macaca radiata, Male, Neurons, Vision, Binocular, Vision, Monocular, Visual Cortex
Show Abstract · Added August 27, 2020
In humans and other primates, sensory signals from each eye remain separated until they arrive in the primary visual cortex (V1), but their exact meeting point is unknown. In V1, some neurons respond to stimulation of only one eye (monocular neurons), while most neurons respond to stimulation of either eye (binocular neurons). The main input layers of V1 contain most of the monocular neurons while binocular neurons dominate the layers above and below. This observation has given rise to the idea that the two eyes' signals remain separate until they converge outside V1's input layers. Here, we show that, despite responding to only one eye, monocular neurons in all layers, including the input layers, of V1 discriminate between stimulation of their driving eye alone and stimulation of both eyes. Some monocular V1 neurons' responses were significantly enhanced, or facilitated, when both eyes were stimulated. Binocular facilitation within V1's input layers tended to occur at the onset of the visual response, which could be explained by converging thalamocortical inputs. However, most V1 monocular neurons were significantly reduced, or suppressed, to binocular stimulation. In contrast to facilitation, binocular suppression occurred several milliseconds following the onset of the visual response, suggesting that the bulk of binocular modulation involves cortical inhibition. These findings, combined, suggest that binocular signals arise at an earlier processing stage than previously appreciated, as even so-called monocular neurons in V1's input layers encode what is shown to both eyes.
Copyright © 2018 Elsevier Ltd. All rights reserved.
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Binocular response modulation in the lateral geniculate nucleus.
Dougherty K, Schmid MC, Maier A
(2019) J Comp Neurol 527: 522-534
MeSH Terms: Action Potentials, Animals, Geniculate Bodies, Humans, Photic Stimulation, Retina, Vision, Binocular, Visual Cortex, Visual Fields, Visual Pathways
Show Abstract · Added August 27, 2020
The dorsal lateral geniculate nucleus of the thalamus (LGN) receives the main outputs of both eyes and relays those signals to the visual cortex. Each retina projects to separate layers of the LGN so that each LGN neuron is innervated by a single eye. In line with this anatomical separation, visual responses of almost all of LGN neurons are driven by one eye only. Nonetheless, many LGN neurons are sensitive to what is shown to the other eye as their visual responses differ when both eyes are stimulated compared to when the driving eye is stimulated in isolation. This, predominantly suppressive, binocular modulation of LGN responses might suggest that the LGN is the first location in the primary visual pathway where the outputs from the two eyes interact. Indeed, the LGN features several anatomical structures that would allow for LGN neurons responding to one eye to modulate neurons that respond to the other eye. However, it is also possible that binocular response modulation in the LGN arises indirectly as the LGN also receives input from binocular visual structures. Here we review the extant literature on the effects of binocular stimulation on LGN spiking responses, highlighting findings from cats and primates, and evaluate the neural circuits that might mediate binocular response modulation in the LGN.
© 2018 Wiley Periodicals, Inc.
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Prefrontal Control of Visual Distraction.
Cosman JD, Lowe KA, Zinke W, Woodman GF, Schall JD
(2018) Curr Biol 28: 414-420.e3
MeSH Terms: Animals, Attention, Evoked Potentials, Macaca mulatta, Male, Prefrontal Cortex, Visual Cortex, Visual Perception
Show Abstract · Added March 15, 2018
Avoiding distraction by conspicuous but irrelevant stimuli is critical to accomplishing daily tasks. Regions of prefrontal cortex control attention by enhancing the representation of task-relevant information in sensory cortex, which can be measured in modulation of both single neurons and event-related electrical potentials (ERPs) on the cranial surface [1, 2]. When irrelevant information is particularly conspicuous, it can distract attention and interfere with the selection of behaviorally relevant information. Such distraction can be minimized via top-down control [3-5], but the cognitive and neural mechanisms giving rise to this control over distraction remain uncertain and debated [6-9]. Bridging neurophysiology to electrophysiology, we simultaneously recorded neurons in prefrontal cortex and ERPs over extrastriate visual cortex to track the processing of salient distractors during a visual search task. Critically, when the salient distractor was successfully ignored, but not otherwise, we observed robust suppression of salient distractor representations. Like target selection, the distractor suppression was observed in prefrontal cortex before it appeared over extrastriate cortical areas. Furthermore, all prefrontal neurons that showed suppression of the task-irrelevant distractor also contributed to selecting the target. This suggests a common prefrontal mechanism is responsible for both selecting task-relevant and suppressing task-irrelevant information in sensory cortex. Taken together, our results resolve a long-standing debate over the mechanisms that prevent distraction, and provide the first evidence directly linking suppressed neural firing in prefrontal cortex with surface ERP measures of distractor suppression.
Copyright © 2017 Elsevier Ltd. All rights reserved.
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8 MeSH Terms
Spiking Suppression Precedes Cued Attentional Enhancement of Neural Responses in Primary Visual Cortex.
Cox MA, Dougherty K, Adams GK, Reavis EA, Westerberg JA, Moore BS, Leopold DA, Maier A
(2019) Cereb Cortex 29: 77-90
MeSH Terms: Action Potentials, Animals, Attention, Cues, Macaca mulatta, Macaca radiata, Male, Photic Stimulation, Random Allocation, Reaction Time, Visual Cortex
Show Abstract · Added August 27, 2020
Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naïve subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses.
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Convergent individual differences in visual cortices, but not the amygdala across standard amygdalar fMRI probe tasks.
Villalta-Gil V, Hinton KE, Landman BA, Yvernault BC, Perkins SF, Katsantonis AS, Sellani CL, Lahey BB, Zald DH
(2017) Neuroimage 146: 312-319
MeSH Terms: Adult, Affect, Amygdala, Brain Mapping, Facial Expression, Facial Recognition, Female, Humans, Individuality, Magnetic Resonance Imaging, Male, Photic Stimulation, Visual Cortex, Young Adult
Show Abstract · Added April 6, 2017
The amygdala (AMG) has been repeatedly implicated in the processing of threatening and negatively valenced stimuli and multiple fMRI paradigms have reported personality, genetic, and psychopathological associations with individual differences in AMG activation in these paradigms. Yet the interchangeability of activations in these probes has not been established, thus it remains unclear if we can interpret AMG responses on specific tasks as general markers of its reactivity. In this study we aimed to assess if different tasks that have been widely used within the Affective Neuroscience literature consistently recruit the AMG.
METHOD - Thirty-two young healthy subjects completed four fMRI tasks that have all been previously shown to probe the AMG during processing of threatening stimuli: the Threat Face Matching (TFM), the Cued Aversive Picture (CAP), the Aversive and Erotica Pictures (AEP) and the Screaming Lady paradigm (SLp) tasks. Contrasts testing response to aversive stimuli relative to baseline or neutral stimuli were generated and correlations between activations in the AMG were calculated across tasks were performed for ROIs of the AMG.
RESULTS - The TFM, CAP and AEP, but not the SLp, successfully recruit the AMG, among other brain regions, especially when contrasts were against baseline or nonsocial stimuli. Conjunction analysis across contrasts showed that visual cortices (VisCtx) were also consistently recruited. Correlation analysis between the extracted data for right and left AMG did not yield significant associations across tasks. By contrast, the extracted signal in VisCtx showed significant associations across tasks (range r=0.511-r=0.630).
CONCLUSIONS - Three of the four paradigms revealed significant AMG reactivity, but individual differences in the magnitudes of AMG reactivity were not correlated across paradigms. By contrast, VisCtx activation appears to be a better candidate than the AMG as a measure of individual differences with convergent validity across negative emotion processing paradigms.
Copyright © 2016 Elsevier Inc. All rights reserved.
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14 MeSH Terms
Correlated activity of cortical neurons survives extensive removal of feedforward sensory input.
Shapcott KA, Schmiedt JT, Saunders RC, Maier A, Leopold DA, Schmid MC
(2016) Sci Rep 6: 34886
MeSH Terms: Animals, Female, Macaca mulatta, Neurons, Neurophysiological Monitoring, Photic Stimulation, Visual Cortex
Show Abstract · Added August 27, 2020
A fundamental property of brain function is that the spiking activity of cortical neurons is variable and that some of this variability is correlated between neurons. Correlated activity not due to the stimulus arises from shared input but the neuronal circuit mechanisms that result in these noise correlations are not fully understood. Here we tested in the visual system if correlated variability in mid-level area V4 of visual cortex is altered following extensive lesions of primary visual cortex (V1). To this end we recorded longitudinally the neuronal correlations in area V4 of two behaving macaque monkeys before and after a V1 lesion while the monkeys fixated a grey screen. We found that the correlations of neuronal activity survived the lesions in both monkeys. In one monkey, the correlation of multi-unit spiking signals was strongly increased in the first week post-lesion, while in the second monkey, correlated activity was slightly increased, but not greater than some week-by-week fluctuations observed. The typical drop-off of inter-neuronal correlations with cortical distance was preserved after the lesion. Therefore, as V4 noise correlations remain without feedforward input from V1, these results suggest instead that local and/or feedback input seem to be necessary for correlated activity.
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