Neural activity in primate parietal area 7a related to spatial analysis of visual mazes

Cognitive psychological studies of humans and monkeys solving visual mazes have provided evidence that a covert analysis of the maze takes place during periods of eye fixation interspersed between saccades, or when mazes are solved without eye movements. We investigated the neural basis of this process in posterior parietal cortex by recording the activity of single neurons in area 7a during maze solution. Monkeys were required to determine from a single point of fixation whether a critical path through the maze reached an exit or a blind ending. We found that during this process the activity of approximately one in four neurons in area 7a was spatially tuned to maze path direction. We obtained evidence that path tuning did not reflect a covert saccade plan insofar as the majority of neurons active during maze solution were not active on a delayed-saccade control task, and the minority that were active on both tasks did not exhibit congruent spatial tuning in the two conditions. We also obtained evidence that path tuning during maze solution was not due to the locations of visual receptive fields mapped outside the behavioral context of maze solution, in that receptive field centers and preferred path directions were not spatially aligned. Finally, neurons tuned to path direction were not present in area 7a when a na?ve animal viewed the same visual maze stimuli but did not solve them. These data support the hypothesis that path tuning in parietal cortex is not due to the lower level visual features of the maze stimulus, but rather is associated with maze solution, and as such, reflects a cognitive process applied to a complex visual stimulus.     

Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey

We examined the nature and the selectivity of the motion deficitsproduced by lesions of extrastriate areas MT and MST. Lesionswere made by injecting ibotenic acid into the representationof the left visual field in two macaque monkeys. The monkeysdiscriminated two stimuli that differed either in stimulus directionor orientation. Direction and orientation discrimination wereassessed by measuring thresholds with gratings and random-dotsplaced in the intact or lesioned visual fields. At the startof behavioral testing, we found pronounced, motion-specificdeficits in thresholds for all types of moving stimuli, includingpronounced elevations in contrast thresholds and in signal-to-noisethresholds measured with moving gratings, as well as deficitsin direction range thresholds and motion coherence measuredwith random-dot stimuli. In addition, the accuracy of directiondiscrimination was reduced at smaller spatial displacements(i.e. step sizes), suggesting an increase in spatial scale ofthe residual directional mechanism. Subsequent improve- mentsin thresholds were seen with all motion stimuli, as behavioraltraining progressed, and these improvements occurred only withextensive behavioral testing in the lesioned visual field. Theseimprovements were particularly pronounced for stimuli not maskedby noise. On the other hand, deficits in the ability to extractmotion from noisy stimuli and in the accuracy of direction discriminationpersisted despite extensive behavioral training. These resultsdemonstrate the importance of areas MT and MST for the perceptionof motion direction, particularly in the presence of noise.In addition, they provide evidence for the importance of behavioraltraining for functional recovery after cortical lesions. Thedata also strongly support the idea of functional specializationof areas MT and MST for motion processing.     

Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex.

Functional magnetic resonance imaging (fMRI) was used to estimate the average receptive field sizes of neurons in each of several striate and extrastriate visual areas of the human cerebral cortex. The boundaries of the visual areas were determined by retinotopic mapping procedures and were visualized on flattened representations of the occipital cortex. Estimates of receptive field size were derived from the temporal duration of the functional activation at each cortical location as a visual stimulus passed through the receptive fields represented at that location. Receptive fields are smallest in the primary visual cortex (V1). They are larger in V2, larger again in V3/VP and largest of all in areas V3A and V4. In all these areas, receptive fields increase in size with increasing stimulus eccentricity. The results are qualitatively in line with those obtained by others in macaque monkeys using neurophysiological methods.     

Structure of the excitatory receptive fields of infragranular forelimb neurons in the rat primary somatosensory cortex responding to touch

We quantitatively studied the excitatory receptive fields of 297 neurons recorded from the forelimb infragranular somatosensory cortex of the rat while touch stimuli were applied to discrete locations on the forelimbs. Receptive fields were highly heterogeneous, but they were regulated, on average, by an underlying spatio-temporal structure. We found the following. (i) Neurons responded with decreasing magnitude and increasing latency when the stimulus was moved from the primary location to secondary locations and to far ispilateral locations of their excitatory receptive fields, displaying smooth transitions from the primary location to secondary locations. (ii) Receptive field patterns revealed functional connectivity between the digits and ventral palm, which did not depend on whether the digits were stimulated dorsally or ventrally. (iii) The structure of the receptive fields (i.e. the neural responses to stimulation of secondary locations compared to the neural responses to stimulation of the primary location), reflected cortical (rather than body) distances. (iv) There was a functional separation between the forepaw and the rest of the forelimb. Namely: if the primary location was in the digits or palm, secondary locations were biased toward the digits and palm; if the primary location was in rest of the forelimb, secondary locations appeared equally distributed over forelimb, digits and palm. (v) More than 40% of neurons extended their receptive field to the ipsilateral forelimb, without any evident spatial organization. Overall, the stimuli evoked approximately 3 times more spikes from secondary responses than from primary responses. These results suggest that a rich repertoire of spatio-temporal responses is available for encoding tactile information. This highly distributed receptive field structure provides the electrophysiological architecture for studying organization and plasticity of cortical somatosensory processing.     

Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkey

Perception of two- and three-dimensional optic flow critically depends upon extrastriate cortices that are part of the 'dorsal stream' for visual processing. Neurons in area 7a, a sub-region of the posterior parietal cortex, have a dual sensitivity to visual input and to eye position. The sensitivity and selectivity of area 7a neurons to three sensory cues - optic flow, retinotopic stimulus position and eye position - were studied. The visual response to optic flow was modulated by the retinotopic stimulus position and by the eye position in the orbit. The position dependence of the retinal and eye position modulation (i.e. gain field) were quantified by a quadratic regression model that allowed for linear or peaked receptive fields. A local maximum (or minimum) in both the retinotopic fields and the gain fields was observed, suggesting that these sensory qualities are not necessarily linearly represented in area 7a. Neurons were also found that simply encoded the eye position in the absence of optic flow. The spatial tuning for the eye position signals upon stationary stimuli and optic flow was not the same, suggesting multiple anatomical sources of the signals. These neurons can provide a substrate for spatial representation while primates move in the environment.      

Neural responses during interception of real and apparent circularly moving stimuli in motor cortex and area 7a

We recorded the neuronal activity in the arm area of the motor cortex and parietal area 7a of two monkeys during interception of stimuli moving in real and apparent motion. The stimulus moved along a circular path with one of five speeds (180-540 degrees/s), and was intercepted at 6 o'clock by exerting a force pulse on a semi-isometric joystick which controlled a cursor on the screen. The real stimuli were shown in adjacent positions every 16 ms, whereas in the apparent motion situation five stimuli were flashed successively at the vertices of a regular pentagon. The results showed, first, that a group of neurons in both areas above responded not only during the interception but also during a NOGO task in which the same stimuli were presented in the absence of a motor response. This finding suggests these areas are involved in both the processing of the stimulus as well as in the preparation and production of the interception movement. In addition, a group of motor cortical cells responded during the interception task but not during a center --> out task, in which the monkeys produced similar force pulses towards eight stationary targets. This group of cells may be engaged in sensorimotor transformations more specific to the interception of real and apparent moving stimuli. Finally, a multiple regression analysis revealed that the time-varying neuronal activity in area 7a and motor cortex was related to various aspects of stimulus motion and hand force in both the real and apparent motion conditions, with stimulus-related activity prevailing in area 7a and hand-related activity prevailing in motor cortex. In addition, the neural activity was selectively associated with the stimulus angle during real motion, whereas it was tightly correlated to the time-to-contact in the apparent motion condition, particularly in the motor cortex. Overall, these observations indicate that neurons in motor cortex and area 7a are processing different parameters of the stimulus depending on the kind of stimulus motion, and that this information is used in a predictive fashion in motor cortex to trigger the interception movement.     

Modulation of visual responses in macaque frontal eye field during covert tracking of invisible targets

The purpose of this study was to investigate the interaction between internal representations of invisible moving targets and visual responses of neurons in frontal eye fields (FEFs). Monkeys were trained to make saccades to the extrapolated position of a target that was temporarily rendered invisible for variable durations as if it had passed behind an occluder. Flashed, task-irrelevant visual probe stimuli were used to study the visual responsiveness of FEF neurons during this task. Probes were flashed at various times and locations during the occlusion interval. Net changes in neuronal activity were obtained by comparing the activity on trials with probes with randomly interleaved trials without any probe. Most neurons showed an increase in firing rate in response to the probe, but some showed a decrease. Both types of responses were enhanced when the invisible target moved toward the receptive field (RF) as compared with trials on which the target moved away from the RF. Some neurons showed a spatial shift in the visual response during the occlusion interval. For cells that were excited by the probe, the shift tended to be correlated with the direction of motion of the target, whereas for cells that were inhibited the shift tended to be in the opposite direction. These results suggest that the role of FEF in predicting invisible target motion includes a sensory/perceptual component.     

Cortical response field dynamics in cat visual cortex

Little is known about the "inverse" of the receptive field--the region of cortical space whose spatiotemporal pattern of electrical activity is influenced by a given sensory stimulus. We refer to this activated area as the cortical response field, the properties of which remain unexplored. Here, the dynamics of cortical response fields evoked in visual cortex by small, local drifting-oriented gratings were explored using voltage-sensitive dyes. We found that the cortical response field was often characterized by a plateau of activity, beyond the rim of which activity diminished quickly. Plateau rim location was largely independent of stimulus orientation. However, approximately 20 ms following plateau onset, 1-3 peaks emerged on it and were amplified for 25 ms. Spiking was limited to the peak zones, whose location strongly depended on stimulus orientation. Thus, alongside selective amplification of a spatially restricted suprathreshold response, wider activation to just below threshold encompasses all orientation domains within a well-defined retinotopic vicinity of the current stimulus, priming the cortex for processing of subsequent stimuli.     

Areas PMLS and 21 a of Cat Visual Cortex: Two Functionally Distinct Areas

We have compared the receptive field properties of neurons recordedfrom visuotopically corresponding regions of area 21a and theposteromedial lateral suprasylvian area (PMLS) of cat visualcortex. In both areas, the great majority of neurons were orientation-selectiveand binocular, and their responses to moving contours were modulatedby simultaneous in-phase or anti-phase motion of large texturedbackground stimuli (‘visual noise’). However, despitethe great hodological similarity between the two areas, PMLSneurons had on average significantly higher peak discharge rates,exhibited substantially greater direction selectivity indices,and preferred substantially higher stimulus velocities thanarea 21a neurons. Furthermore, the majority of binocular neuronsin the PMLS area and in area 21a were dominated respectivelyby the contralateral and the ipsilateral eyes. Finally, while46% of PMLS neurons were excited by movement of visual noiseper Se. only 25% of area 21 a neurons could be excited by suchstimuli. We argue that the PMLS area, like its presumed primatehomologue the middle-temporal (MT) area, is mainly involvedin motion analysis. By contrast, area 21a appears to be involvedin pattern analysis rather than motion analysis. It is likelythat phylogenetically area 21a derives from the PMLS area.     

Visual modulation of neurons in auditory cortex

Our brain integrates the information provided by the different sensory modalities into a coherent percept, and recent studies suggest that this process is not restricted to higher association areas. Here we evaluate the hypothesis that auditory cortical fields are involved in cross-modal processing by probing individual neurons for audiovisual interactions. We find that visual stimuli modulate auditory processing both at the level of field potentials and single-unit activity and already in primary and secondary auditory fields. These interactions strongly depend on a stimulus' efficacy in driving the neurons but occur independently of stimulus category and for naturalistic as well as artificial stimuli. In addition, interactions are sensitive to the relative timing of audiovisual stimuli and are strongest when visual stimuli lead by 20-80 msec. Exploring the underlying mechanisms, we find that enhancement correlates with the resetting of slow (approximately 10 Hz) oscillations to a phase angle of optimal excitability. These results demonstrate that visual stimuli can modulate the firing of neurons in auditory cortex in a manner that depends on stimulus efficacy and timing. These neurons thus meet the criteria for sensory integration and provide the auditory modality with multisensory contextual information about co-occurring environmental events.     

Electrophysiological evidence for fast visual processing through the human koniocellular pathway when stimuli move

There is increasing evidence from cellular recordings in primates and behavioral studies in humans that motion can be processed by other than the magnocellular (M) pathway and the cortical dorsal stream. Little is known about cortical processing of moving stimuli when the information is conveyed by the third retinogeniculocortical pathway - the so-called koniocellular (K) pathway. We addressed this issue in humans by studying the spatio-temporal dynamics of the brain electrical fields evoked by tritan (S-cone isolating) and luminance-defined moving stimuli. Tritan and luminance stimuli are presumably carried by the K and M pathways respectively. We found two time intervals where significant stimulus-specific electric fields were evoked: an early period between 40 and 75 ms after stimulus onset, and a later period between 175 and 240 ms. Some of these fields were identical for tritanand luminance-motion, suggesting that the processing of moving stimuli share common cortical substrates when mediated via K and M pathway input. However, tritan-motion stimuli also evoked unique electric fields that appeared earlier in time than the common motion-specific fields, indicating very fast activation of cortical areas specific to input through the K pathway. A distributed source localization procedure revealed simultaneous activation of striate and extrastriate areas even at the early processing stages, strongly suggesting a very fast activation of the visual cerebral network.     

A neural model of motion processing and visual navigation by cortical area MST

Cells in the dorsal medial superior temporal cortex (MSTd) process optic flow generated by self-motion during visually guided navigation. A neural model shows how interactions between well-known neural mechanisms (log polar cortical magnification, Gaussian motion-sensitive receptive fields, spatial pooling of motion-sensitive signals and subtractive extraretinal eye movement signals) lead to emergent properties that quantitatively simulate neurophysiological data about MSTd cell properties and psychophysical data about human navigation. Model cells match MSTd neuron responses to optic flow stimuli placed in different parts of the visual field, including position invariance, tuning curves, preferred spiral directions, direction reversals, average response curves and preferred locations for stimulus motion centers. The model shows how the preferred motion direction of the most active MSTd cells can explain human judgments of self-motion direction (heading), without using complex heading templates. The model explains when extraretinal eye movement signals are needed for accurate heading perception, and when retinal input is sufficient, and how heading judgments depend on scene layouts and rotation rates.     

Integration of local features to a global percept by neural coupling

The integration of different visual attributes into the percept of a single global shape is a central aspect of object processing. In hierarchically organized stimuli with local and global levels, the attentional focus largely determines which level is processed. Here we tested the hypothesis that object processing during attention to the global aspect of the stimulus is characterized by an increased neural coupling between visual areas reflecting the integration of local features. In the present experiment, we used global letters that were constructed by smaller local letters, and a cue signaled which spatial level should be identified. On the local level, only 1 relevant letter was presented laterally in 1 visual hemifield. In contrast, the global letter extended into both hemifields, and the integration of information from both hemispheres was necessary to identify the global stimulus. Therefore, we expected an increased functional coupling between hemispheres during global processing. This hypothesis was investigated using electroencephalographic recordings and an analysis of phase locking and coherence. The results show that stimulus-locked neural coupling within the gamma band (30-40 Hz) across hemispheres in visual cortex increased for global processing after stimulus presentation and could therefore reflect the integration of local visual information.     

FEF TMS affects visual cortical activity

We tested whether the frontal eye field (FEF) is critical in controlling visual processing in posterior visual brain areas during the orienting of spatial attention. Short trains (5 pulses at 10 Hz) of transcranial magnetic stimulation (TMS) were applied to the right FEF during the cueing period of a covert attentional task while event-related potentials (ERPs) were simultaneously recorded from lateral posterior electrodes, where visual components are prominent. FEF TMS significantly affected the neural activity evoked by visual stimuli, as well as the ongoing neural activity recorded during earlier anticipation of the visual stimuli. The effects of FEF TMS started earlier and were greatest for brain activity recorded ipsilaterally to FEF TMS and contralaterally to the visual stimulus. The TMS-induced effect on visual ERPs occurred at the same time as ERPs were shown to be modulated by visual attention. Importantly, no similar effects were observed after TMS of a control site that was physically closer but not anatomically interconnected to the recording sites. The results show that the human FEF has a causal influence over the modulation of visual activity in posterior areas when attention is being allocated.     

Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex

Visual cortical lesions destroy the target cells for geniculocortical fibers from a certain retinotopic region. This leads to a cortical scotoma. We have investigated the receptive fields of cells in the visual cortex before, 2 days and 2 months after focal ibotenic acid lesions in the adult cat visual cortex and have found signs of receptive field plasticity in the surroundings of the chronic but not the acute and subacute excitotoxic lesions. In the subacute state (first two days post lesion) receptive field sizes of cells at the border of the lesion were reduced in size or remained unchanged. Remapping of cortical receptive fields 2 months later revealed a number of cells with multifold enlarged receptive fields at the border of the lesion. The cells with enlarged receptive fields displayed orientation and direction selectivity like normal cells. The size increase appeared not specifically directed towards the scotoma; however, the enlarged receptive fields can reduce the extent of a cortical scotoma, since previously unresponsive regions of the visual field activate cortical cells at the border of the lesion. This late receptive field plasticity could serve as a mechanism for the filling-in of cortical scotomata observed in patients with visual cortex lesions.     

Neuronal responses in area 7a to multiple-stimulus displays: I. neurons encode the location of the salient stimulus.

The primate posterior parietal cortex (PPC) plays an important role in representing and recalling spatial relationships and in the ability to orient visual attention. This is evidenced by the parietal activation observed in brain imaging experiments performed during visuo- spatial tasks, and by the contralateral neglect syndrome that often accompanies parietal lesions. Individual neurons in monkey parietal cortex respond vigorously to the appearance of single, behaviorally relevant stimuli, but little is known about how they respond to more complex visual displays. The current experiments addressed this issue by recording activity from single neurons in area 7a of the PPC in monkeys performing a spatial version of a match-to-sample task. The task required them to locate salient stimuli in multiple-stimulus displays and release a lever after a subsequent stimulus appeared at the same location. Neurons responded preferentially to the appearance of salient stimuli inside their receptive fields. The presence of multiple stimuli did not affect appreciably the spatial tuning of responses in the majority of neurons or the population code for the location of the salient stimulus. Responses to salient stimuli could be distinguished from background stimuli approximately 100 ms after the onset of the cue. These results suggest that area 7a neurons represent the location of the stimulus attracting the animal's attention and can provide the spatial information required for directing attention to a salient stimulus in a complex scene.     

Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections

The relationships between the distribution of visuomanual signals in parietal cortex and that of parieto-frontal projections are the subject of the present study. Single cell recording was performed in areas PEc and V6A, where different anatomical tracers were also injected. The monkeys performed a variety of behavioral tasks, aimed at studying the visual and motor properties of parietal cells, as well as the potential combination of retinal-, eye- and hand-related signals on cell activity. The activity of most cells was related to the direction of movement and the active position of the hand. Many of these reach-related cells were influenced by eye position information. Fewer cells displayed relationships to saccadic eye movements. The activity of most neurons related to a combination of both hand and eye signals. Many cells were also modulated during preparation for hand movement. Light-dark differences of activity were common and interpreted as related to the sight and monitoring of hand motion and/or position in the visual field. Most cells studied were very sensitive to moving visual stimuli and also responded to optic flow stimulation. Visual receptive fields were generally large and extended to the periphery of the visual field. For most neurons, the orientation of the preferred directions computed across different epochs and tasks conditions clustered within a limited sector of space, the field of global tuning. This can be regarded as an ideal frame to combine spatially congruent eye- and hand-related information for different forms of visuomanual behavior. All these properties were common to both PEc and V6A. Retinal, eye- and hand-related activity types, as well as parieto-frontal association cells, were distributed in a periodic fashion across the tangential domain of areas PEc and V6A. These functional and anatomical distributions were characterized and compared through a spectral and coherency analysis, which revealed the existence of a selective 'match' between activity types and parieto-frontal connections. This match depended on where each individual efferent projection was addressed. The results of the present and of the companion study can be relevant for a re-interpretation of optic ataxia as the consequence of the breakdown of the combination of retinal-, eye- and hand-related directional signals within the global tuning fields of parietal neurons.     

Neuronal responses in area 7a to multiple stimulus displays: II. responses are suppressed at the cued location.

Everyday visual scenes contain a variety of stimuli that vary in their significance. The companion paper demonstrates that neurons in the posterior parietal cortex (PPC) are capable of encoding the spatial locations of the salient stimulus in multiple stimulus scenes. The present experiment sought to address how neuronal responses to stimuli appearing in the receptive field are modulated after attention has been drawn to one of multiple stimuli in a visual scene. We recorded from area 7a of the PPC in monkeys trained to do a spatial version of a match-to-sample task. The results show that neuronal responses are greatly suppressed when stimuli appear at previously attended locations. No reduction in responsiveness is observed for locations where stimuli had previously appeared but did not draw attention. These results support the hypothesis that area 7a has a role in redirecting attention to stimuli appearing at novel, unattended locations.     

Oculocentric Spatial Representation in Parietal Cortex

Parietal cortex comprises several distinct areas. Neurons ineach area are selective for particular stimulus dimensions andparticular regions of space. The representation of space ina given area reflects a particular motor output by which a stimuluscan be acquired. Neurons in the lateral intraparietal area (UP)are active in relation to both visual and motor events. UP neuronsdo not transmit an unambiguous sac-cadic command. Rather theysignal the location at which an event has occurred. These spatiallocations are encoded in oculocentric coordinates, that is,with respect to the current or anticipated position of the centerof gaze. When an eye movement brings the spatial location ofa recently flashed stimulus into the receptive field of an UPneuron, the neuron responds to the memory trace of that stimulus.This result indicates that for nearly all UP neurons, storedvisual information is remapped in conjunction with saccades.Remapping of the memory trace maintains the alignment betweenthe current image on the retina and the stored representationin cortex. Further when an eye movement is about to occur, morethan a third of UP neurons transiently shift the location oftheir receptive fields. This anticipatory remapping allows theneuron to begin to respond to a visual stimulus even beforethe saccade is initiated that will bring the stimulus into thefixation-defined receptive field. Both kinds of remapping serveto create a constantly updated representation of stimulus locationthat is always in terms of distance and direction from the fovea.This oculocentric representation has the advantage that it alreadymatches that known to exist in the frontal eye fields and thesuperior colliculus, the output targets of UP, and it does notrequire further coordinate transformation in order to contributeto spatially accurate behavior. These results indicate thatUP can analyze visual space without ever forming a representationof absolute target position.     

Local cortical function after uncomplicated subdural electrode implantation. Laboratory investigation

OBJECTIVES: Although subdural electrodes are routinely used to map regional brain function, it is unknown if the presence of these implants hinders local cortical function. The authors used psychophysical methods to measure the effect of uncomplicated electrode implantation on local cortical function. METHODS: Local field potentials were used to map receptive fields (RFs) for subdural electrodes that were unilaterally implanted on early visual cortex in 4 patients. After electrode implantation, patients did a task that required them to detect an orientation change in a flashing visual stimulus that was presented either inside the mapped RF or outside the RF in the diametrically opposite portion of the other hemifield. The size of the orientation change was varied to span a wide range of behavioral performance. Psychometric curves were generated by fitting behavioral responses to a logistic function. The threshold was defined as the point at which the fitted function crossed 50% detection. RESULTS: Data were well fit by the logistic function in all 4 patients for both RF and non-RF conditions. None of the volunteers tested showed a statistically significant difference in detection threshold, reaction time, or in the slope of the psychometric function for stimuli presented inside or outside the RF. CONCLUSIONS: Subdural electrodes implanted for extraoperative monitoring do not impair psychophysical performance for a task based on stimuli lying within the RF for recording electrodes. This finding suggests that these electrodes can be used reliably for accurate assessment of regional neurological function.