Rebecca A. Berman

Cortical networks subserving pursuit and saccadic eye movements in humans: an FMRI study.

High‐field (3 Tesla) functional magnetic resonance imaging (MRI) was used to investigate the cortical circuitry subserving pursuit tracking in humans and compare it to that for saccadic eye movements. Pursuit performance, relative to visual fixation, elicited activation in three areas known to contribute to eye movements in humans and in nonhuman primates: the frontal eye field, supplementary eye field, and intraparietal sulcus. It also activated three medial regions not previously identified in human neuroimaging studies of pursuit: the precuneus and the anterior and posterior cingulate cortices. All six areas were also activated during saccades. The spatial extent of activation was similar for saccades and pursuit in all but two regions: spatial extent was greater for saccades in the superior branch of the frontal eye field and greater for pursuit in posterior cingulate cortex. This set of activations for smooth pursuit parallels the network of oculomotor areas characterized in nonhuman primates and complements recent studies showing that common cortical networks subserve oculomotor functions and spatial attention in humans. Hum. Brain Mapping 8:209–225, 1999.

Longitudinal four-dimensional mapping of subcortical anatomy in human development

Significance Our spatiotemporal understanding of subcortical development in humans lags far behind that of the cortical sheet. This disparity ignores that developmental refinements and disruptions of complex behavior involve systems spanning both components of the brain. We begin redressing this imbalance by applying new techniques for striatal, pallidal and thalamic morphometry to large-scale longitudinal neuroimaging data extending from childhood through early adulthood. This work (i) establishes the curvilinear, sexual dimorphic and often protracted nature of global volume change within each structure, (ii) reveals profound spatiotemporal complexities in striatal, pallidal and thalamic maturation that are organized by the known topography of primate cortico-subcortical connectivity, and (iii) identifies focal sex differences in subcortical maturation that strike regions implicated in psychopathologies with an adolescent-emergent sex-bias. Growing access to large-scale longitudinal structural neuroimaging data has fundamentally altered our understanding of cortical development en route to human adulthood, with consequences for basic science, medicine, and public policy. In striking contrast, basic anatomical development of subcortical structures such as the striatum, pallidum, and thalamus has remained poorly described—despite these evolutionarily ancient structures being both intimate working partners of the cortical sheet and critical to diverse developmentally emergent skills and disorders. Here, to begin addressing this disparity, we apply methods for the measurement of subcortical volume and shape to 1,171 longitudinally acquired structural magnetic resonance imaging brain scans from 618 typically developing males and females aged 5–25 y. We show that the striatum, pallidum, and thalamus each follow curvilinear trajectories of volume change, which, for the striatum and thalamus, peak after cortical volume has already begun to decline and show a relative delay in males. Four-dimensional mapping of subcortical shape reveals that (i) striatal, pallidal, and thalamic domains linked to specific fronto-parietal association cortices contract with age whereas other subcortical territories expand, and (ii) each structure harbors hotspots of sexually dimorphic change over adolescence—with relevance for sex-biased mental disorders emerging in youth. By establishing the developmental dynamism, spatial heterochonicity, and sexual dimorphism of human subcortical maturation, these data bring our spatiotemporal understanding of subcortical development closer to that of the cortex—allowing evolutionary, basic, and clinical neuroscience to be conducted within a more comprehensive developmental framework.

Functional Identification of a Pulvinar Path from Superior Colliculus to Cortical Area MT

The idea of a second visual pathway, in which visual signals travel from brainstem to cortex via the pulvinar thalamus, has had considerable influence as an alternative to the primary geniculo-striate pathway. Existence of this second pathway in primates, however, is not well established. A major question centers on whether the pulvinar acts as a relay, particularly in the path from the superior colliculus (SC) to the motion area in middle temporal cortex (MT). We used physiological microstimulation to identify pulvinar neurons belonging to the path from SC to MT in the macaque. We made three salient observations. First, we identified many neurons in the visual pulvinar that received input from SC or projected to MT, as well as a largely separate set of neurons that received input from MT. Second, and more importantly, we identified a subset of neurons as relay neurons that both received SC input and projected to MT. The identification of these relay neurons demonstrates a continuous functional path from SC to MT through the pulvinar in primates. Third, we histologically localized a subset of SC–MT relay neurons to the subdivision of inferior pulvinar known to project densely to MT but also localized SC–MT relay neurons to an adjacent subdivision. This pattern indicates that the pulvinar pathway is not limited to a single anatomically defined region. These findings bring new perspective to the functional organization of the pulvinar and its role in conveying signals to the cerebral cortex.

Inhibitory control of attention declines more than working memory during normal aging

Changes in frontostriatal systems are believed to reduce the efficiency of executive cognitive functions during normal aging, especially the inhibitory control of attentional and behavioral responses. To characterize changes during normal aging in sensorimotor, working memory and inhibitory attentional systems, we tested 20 healthy elderly subjects (age 65-80) and 28 young adults (age 18-34) using oculomotor paradigms. Visually guided saccades of elderly subjects showed decreased peak velocity and increased reaction time, but not reduced accuracy, indicating selective age-related declines in sensorimotor systems. In an oculomotor working memory task, memory for spatial location information in elderly subjects was as accurate as in young adults. In contrast, elderly subjects demonstrated a significantly reduced ability to voluntarily inhibit eye movements toward flashed targets on an antisaccade task. These findings indicate changes in frontostriatal systems during normal aging that adversely affect volitional inhibitory processes but spare encoding and retrieval components of spatial working memory.

Signals Conveyed in the Pulvinar Pathway from Superior Colliculus to Cortical Area MT

We previously established a functional pathway extending from the superficial layers of the superior colliculus (SC) through the inferior pulvinar (PI) to cortical area MT in the primate (Macaca mulatta). Here, we characterized the signals that this pathway conveys to cortex by recording from pulvinar neurons that we identified by microstimulation as receiving input from SC and/or projecting to MT. The basic properties of these ascending-path PI neurons resembled those of SC visual neurons. Namely, they had brisk responses to spots of light, inhibitory surrounds, and relatively large receptive fields that increased with eccentricity, as well as minimal presaccadic activity. Beyond these basic properties, there were two salient results regarding the modulatory and motion signals conveyed by this ascending pathway. First, the PI neurons appeared to convey only a subset of the modulations found in the SC: they exhibited saccadic suppression, the inhibition of activity at the time of the saccade, but did not clearly show the attentional enhancement of the visual response seen in SC. Second, directional selectivity was minimal in PI neurons belonging to the ascending path but was significantly more prominent in PI neurons receiving input from MT. This finding casts doubt on earlier assumptions that PI provides directionally selective signals to MT and instead suggests that PI derives its selectivity from MT. The identification of this pathway and its transmitted activity establishes the first functional pathway from brainstem to cortex through pulvinar and makes it possible to examine its contribution to cortical visual processing, perception, and action.

Neuronal mechanisms for visual stability: progress and problems

How our vision remains stable in spite of the interruptions produced by saccadic eye movements has been a repeatedly revisited perceptual puzzle. The major hypothesis is that a corollary discharge (CD) or efference copy signal provides information that the eye has moved, and this information is used to compensate for the motion. There has been progress in the search for neuronal correlates of such a CD in the monkey brain, the best animal model of the human visual system. In this article, we briefly summarize the evidence for a CD pathway to frontal cortex, and then consider four questions on the relation of neuronal mechanisms in the monkey brain to stable visual perception. First, how can we determine whether the neuronal activity is related to stable visual perception? Second, is the activity a possible neuronal correlate of the proposed transsaccadic memory hypothesis of visual stability? Third, are the neuronal mechanisms modified by visual attention and does our perceived visual stability actually result from neuronal mechanisms related primarily to the central visual field? Fourth, does the pathway from superior colliculus through the pulvinar nucleus to visual cortex contribute to visual stability through suppression of the visual blur produced by saccades?

Optogenetic Inactivation Modifies Monkey Visuomotor Behavior

A critical technique for understanding how neuronal activity contributes to behavior is determining whether perturbing it changes behavior. The advent of optogenetic techniques allows the immediately reversible alteration of neuronal activity in contrast to chemical approaches lasting minutes to hours. Modification of behavior using optogenetics has had substantial success in rodents but has not been as successful in monkeys. Here, we show how optogenetic inactivation of superior colliculus neurons in awake monkeys leads to clear and repeatable behavioral deficits in the metrics of saccadic eye movements. We used our observations to evaluate principles governing the use of optogenetic techniques in the study of the neuronal bases of behavior in monkeys, particularly how experimental design must address relevant parameters, such as the application of light to subcortical structures, the spread of viral injections, and the extent of neuronal inactivation with light.

Thalamic pathways for active vision

Active vision requires the integration of information coming from the retina with that generated internally within the brain, especially by saccadic eye movements. Just as visual information reaches cortex via the lateral geniculate nucleus of the thalamus, this internal information reaches the cerebral cortex through other higher-order nuclei of the thalamus. This review summarizes recent work on four of these thalamic nuclei. The first two pathways convey internal information about upcoming saccades (a corollary discharge) and probably contribute to the neuronal mechanisms that underlie stable visual perception. The second two pathways might contribute to the neuronal mechanisms underlying visual spatial attention in cortex and in the thalamus itself.

Auditory and visual attention modulate motion processing in area MT

Behavioral and physiological studies have established that visual attention to a given feature or location can modulate early visual processing. In the present experiment, we asked whether auditory attention can likewise influence visual processing. We used a visual illusion, the motion aftereffect (MAE), to assess the effects of visual and auditory attention on motion processing in human area MT+. We acquired psychophysical and functional magnetic resonance imaging (fMRI) data while subjects fixated and viewed moving and stationary stimuli in alternating blocks. For each of four motion conditions, we measured the duration of the subsequent MAE, the time for activity in MT+ to return to baseline after motion adaptation (decay time), and the magnitude of MT+ activity during motion adaptation. For each subject, we first obtained measures of motion processing in the absence of attentional demands, by comparing reversing and expanding motion conditions. Subjects perceived the MAE following adaptation to expanding but not reversing motion, as observed previously, and decay times in MT+ were selectively prolonged after expanding motion. We then assessed the effects of performing either a visual or an auditory attentional task during expanding motion adaptation. Performance of the attentional task, whether visual or auditory, produced a significant reduction of subsequent MAE perception and associated decay times in MT+, as compared to expanding motion with fixation only. Both attentional tasks also reduced the magnitude of activation during motion adaptation. These data show that auditory attention, like visual attention, can modify sensory processing at a remarkably early stage of the visual hierarchy.

Attention and active vision.

Visual perception results from the interaction of incoming sensory signals and top down cognitive and motor signals. Here we focus on the representation of attended locations in parietal cortex and in earlier visual cortical areas. We review evidence that these spatial representations are modulated not only by selective attention but also by the intention to move the eyes. We describe recent experiments in monkey and human that elucidate the mechanisms and circuitry involved in updating, or remapping, the representations of salient stimuli. Two central ideas emerge. First, selective attention and remapping are closely intertwined, and together contribute to the percept of spatial stability. Second, remapping is accomplished not by a single area but by the participation of parietal, frontal and extrastriate cortex as well as subcortical structures. This neural circuitry is distinguished by significant redundancy and plasticity, suggesting that the updating of salient stimuli is fundamental for spatial stability and visuospatial behavior. We conclude that multiple processes and pathways contribute to active vision in the primate brain.