Neuronal activity in the caudal frontal eye fields of monkeys during memory-based smooth pursuit eye movements: comparison with the supplementary eye fields

Recently, we examined the neuronal substrate of predictive pursuit during memory-based smooth pursuit and found that supplementary eye fields (SEFs) contain signals coding assessment and memory of visual motion direction, decision not-to-pursue ("no-go"), and preparation for pursuit. To determine whether these signals were unique to the SEF, we examined the discharge of 185 task-related neurons in the caudal frontal eye fields (FEFs) in 2 macaques. Visual motion memory and no-go signals were also present in the caudal FEF but compared with those in the SEF, the percentage of neurons coding these signals was significantly lower. In particular, unlike SEF neurons, directional visual motion responses of caudal FEF neurons decayed exponentially. In contrast, the percentage of neurons coding directional pursuit eye movements was significantly higher in the caudal FEF than in the SEF. Unlike SEF inactivation, muscimol injection into the caudal FEF did not induce direction errors or no-go errors but decreased eye velocity during pursuit causing an inability to compensate for the response delays during sinusoidal pursuit. These results indicate significant differences between the 2 regions in the signals represented and in the effects of chemical inactivation suggesting that the caudal FEF is primarily involved in generating motor commands for smooth-pursuit eye movements.     

Physiological responses of New World monkey V1 neurons to stimuli defined by coherent motion

We studied the responses of neurons in area V1 of marmosets to visual stimuli that moved against dynamic textured backgrounds. The stimuli were defined either by a first-order cue ('solid' bars, which were either darker or lighter than the background) or by a second-order cue ('camouflaged' bars, defined only by coherent motion). Forty-two per cent of the neurons demonstrated a similar selectivity for the direction of motion of the solid and camouflaged bars, thereby characterizing a population of cue-invariant (CI) cells. The other cells either showed different selectivity to the movement of solid and camouflaged bars (non-cue-invariant, or NCI cells), or responded equally well to movement in all directions. CI neurons, which were rare in layer 4, tended to have larger receptive fields and to be more strongly direction selective than NCI cells. Although V1 neurons tended to show maximal responses to camouflaged bars that were longer than the 'optimal' solid bars, many CI neurons preferred first- and second-order stimuli of similar lengths. Finally, the activity evoked by the camouflaged bars was delayed in relation to that evoked by solid bars. These results demonstrate that motion CI responses are relatively common in primate V1, especially among a population of strongly direction-selective neurons. They also indicate that this response property may depend on feedback from extrastriate areas, or on complex intrinsic interactions within V1.     

Eye-pursuit and reafferent head movement signals carried by pursuit neurons in the caudal part of the frontal eye fields during head-free pursuit

Eye and head movements are coordinated during head-free pursuit. To examine whether pursuit neurons in frontal eye fields (FEF) carry gaze-pursuit commands that drive both eye-pursuit and head-pursuit, monkeys whose heads were free to rotate about a vertical axis were trained to pursue a juice feeder with their head and a target with their eyes. Initially the feeder and target moved synchronously with the same visual angle. FEF neurons responding to this gaze-pursuit were tested for eye-pursuit of target motion while the feeder was stationary and for head-pursuit while the target was stationary. The majority of pursuit neurons exhibited modulation during head-pursuit, but their preferred directions during eye-pursuit and head-pursuit were different. Although peak modulation occurred during head movements, the onset of discharge usually was not aligned with the head movement onset. The minority of neurons whose discharge onset was so aligned discharged after the head movement onset. These results do not support the idea that the head-pursuit-related modulation reflects head-pursuit commands. Furthermore, modulation similar to that during head-pursuit was obtained by passive head rotation on stationary trunk. Our results suggest that FEF pursuit neurons issue gaze or eye movement commands during gaze-pursuit and that the head-pursuit-related modulation primarily reflects reafferent signals resulting from head movements.     

Tuning curve shift by attention modulation in cortical neurons: a computational study of its mechanisms

Physiological studies of visual attention have demonstrated that focusing attention near a visual cortical neuron's receptive field (RF) results in enhanced evoked activity and RF shift. In this work, we explored the mechanisms of attention induced RF shifts in cortical network models that receive an attentional 'spotlight'. Our main results are threefold. First, whereas a 'spotlight' input always produces toward-attention shift of the population activity profile, we found that toward-attention shifts in RFs of single cells requires multiplicative gain modulation. Secondly, in a feedforward two-layer model, focal attentional gain modulation in first-layer neurons induces RF shift in second-layer neurons downstream. In contrast to experimental observations, the feedforward model typically fails to produce RF shifts in second-layer neurons when attention is directed beyond RF boundaries. We then show that an additive spotlight input combined with a recurrent network mechanism can produce the observed RF shift. Inhibitory effects in a surround of the attentional focus accentuate this RF shift and induce RF shrinking. Thirdly, we considered interrelationship between visual selective attention and adaptation. Our analysis predicts that the RF size is enlarged (respectively reduced) by attentional signal directed near a cell's RF center in a recurrent network (resp. in a feedforward network); the opposite is true for visual adaptation. Therefore, a refined estimation of the RF size during attention and after adaptation would provide a probe to differentiate recurrent versus feedforward mechanisms for RF shifts.     

Cortical neuronal responses to optic flow are shaped by visual strategies for steering

We hypothesized that neuronal responses to virtual self-movement would be enhanced during steering tasks. We recorded the activity of medial superior temporal (MSTd) neurons in monkeys trained to steer a straight-ahead course, using optic flow. We found smaller optic flow responses during active steering than during the passive viewing of the same stimuli. Behavioral analysis showed that the monkeys had learned to steer using local motion cues. Retraining the monkeys to use the global pattern of optic flow reversed the effects of the active-steering task: active steering then evoked larger responses than passive viewing. We then compared the responses of neurons during active steering by local motion and by global patterns: Local motion trials promoted the use of local dot movement near the center of the stimulus by occluding the peripheral visual field midway through the trial. Global pattern trials promoted the use of radial pattern movement by occluding the central visual field midway through the trial. In this study, identical full-field optic-flow stimuli evoked larger responses in global-pattern trials than in local motion trials. We conclude that the selection of specific visual cues reflects strategies for active steering and alters MSTd neuronal responses to optic flow.     

Functional sub-regions for optic flow processing in the posteromedial lateral suprasylvian cortex of the cat.

During locomotion, an observer sees a large and complex pattern of visual motion called optic flow. This phenomenon is characterized by elements in the environment accelerating and expanding as they move peripherally. In cats, previous studies have indicated that the posteromedial part of the lateral suprasylvian (PMLS) cortex may be involved in the processing of optic flow fields. We further addressed this issue by studying the importance of specific parameters of the optic flow patterns and investigating whether cell responses to these stimuli depend on receptive field (RF) location in the visual field. Results can be summarized as follows: approximately two-thirds of PMLS cells responded to optic flow fields and a subset of these (84/153) showed a clear direction selectivity for motion along the frontal axis. Of these units, the majority responded preferentially to expansion rather than contraction of the pattern. Cells' responses depend on RF location in the visual field. For centrally located RFs, tested both when the origin of motion was within the RF or at the area centralis, responses were generally comparable whether or not size or speed gradients were removed from the optic flow pattern. A different tendency was observed for peripherally located RFs. In general, these cells exhibited a preferred direction almost exclusively when the origin of motion was placed at the area centralis, and neuronal discharges and direction selectivity for many of them were reduced when the optic flow cues were removed from the pattern. The results of this study suggest that there may be functional differences in response properties between PMLS cells located in the central and peripheral parts of the visual field that may reflect a specialization of the PMLS cortex in optic flow processing.     

Smooth pursuit-related information processing in frontal eye field neurons that project to the NRTP

The cortical pursuit system begins the process of transforming visual signals into commands for smooth pursuit (SP) eye movements. The frontal eye field (FEF), located in the fundus of arcuate sulcus, is known to play a role in SP and gaze pursuit movements. This role is supported, at least in part, by FEF projections to the rostral nucleus reticularis tegmenti pontis (rNRTP), which in turn projects heavily to the cerebellar vermis. However, the functional characteristics of SP-related FEF neurons that project to rNRTP have never been described. Therefore, we used microelectrical stimulation (ES) to deliver single pulses (50-200 microA, 200-micros duration) in rNRTP to antidromically activate FEF neurons. We estimated the eye or retinal error motion sensitivity (position, velocity, and acceleration) of FEF neurons during SP using multiple linear regression modeling. FEF neurons that projected to rNRTP were most sensitive to eye acceleration. In contrast, FEF neurons not activated following ES of rNRTP were often most sensitive to eye velocity. In similar modeling studies, we found that rNRTP neurons were also biased toward eye acceleration. Therefore, our results suggest that neurons in the FEF-rNRTP pathway carry signals that could play a primary role in initiation of SP.     

The contribution of the human FEF and SEF to smooth pursuit initiation

Smooth pursuit eye movements function to keep moving targets foveated. Behavioral studies have shown that pursuit is particularly effective for predictable target motion. There is evidence that both the frontal eye field (FEF) and supplementary eye field (SEF) (also known as the dorsomedial frontal cortex) contribute to pursuit control. The goal of the current experiment was to determine whether these 2 areas made different contributions to the initiation of pursuit in response to predictable compared with unpredictable target motion. Transcranial magnetic stimulation (TMS) was used in 5 healthy human participants to temporarily disrupt each area around the time of target motion onset. TMS over the FEF delayed contraversive pursuit markedly more than ipsiversive pursuit and this direction-dependent difference was more deeply modulated during pursuit of unpredictable than predictable target motion. By contrast, TMS over the SEF resulted in a much more muted modulation of pursuit latency that was similar across both predictable and unpredictable conditions. Taken together, we conclude that the human FEF, but not the SEF, makes a significant contribution to the processing required during the preparation of contraversive pursuit responses to unpredictable target motion and this contribution is less vital during pursuit to predictable target motion.     

Simultaneous representation of saccade targets and visual onsets in monkey lateral intraparietal area

The monkey's lateral intraparietal area (LIP) has been associated with attention and saccades. LIP neurons have visual on-responses to objects abruptly appearing in their receptive fields (RFs) and sustained activity preceding saccades to the RF. We studied the relationship between the on-responses and delay activity in LIP using a 'stable-array' task. Monkeys viewed eight distinct, continuously illuminated objects, arranged in a circle with at least one object in the RF. A cue flashed instructing the monkey to make a saccade, after a delay, to the stable object physically matching the cue. The location of the cue was fixed in trial blocks, either in or out of the RF. If the cue was outside the RF, neurons developed delay-period activity tuned for the direction of the saccade target at approximately 190 ms after cue onset. If the cue appeared in the RF, neurons initially responded to cue onset and developed tuning for saccade direction only toward the end of the delay period, 390 ms after cue onset. The cue- and saccade-target responses coexisted throughout a significant portion of the delay period. The results show that visual-on responses and delay-period activity in LIP are functionally separable, and that, although highly selective, the salience representation in LIP can contain more than one object at a time.     

Neuronal responses to optic flow in the monkey parietal area PEc

Area PEc, a high order association area, is located in the dorsocaudal portion of the superior parietal cortex. PEc neurons encode visual motion signals, especially the direction of stimulus motion. The present study tested if PEc neurons also process visual correlates of self-motion. The extracellular activity of single neurons in response to optic flow stimuli was recorded in two monkeys (Macaca fascicularis) trained in a fixation task. The stimuli were produced by random dots simulating planar motion, radial expansion and radial contraction. A substantial number of PEc neurons were specifically activated by radial optic flow and were selective for the position of the focus of expansion with respect to the fovea. Eccentric positions of the focus of expansion were preferred. Almost all neurons showed opponent excitatory-inhibitory activity to expanding-contracting visual fields. Planar motion elicited very weak responses. Optic flow responsiveness is not entirely explained by classical bar sensitivity in PEc neurons, suggesting that optic flow and classical bar responses could serve different mechanisms in the integration of visuo-motor signals to prepare body movements.     

Modulation of antisaccades by transcranial magnetic stimulation of the human frontal eye field

It has been suggested that the frontal eye field (FEF), which is involved with the inhibition and generation of saccades, is engaged to a different degree in pro- and antisaccades. Pro- and antisaccades are often assessed in separate experimental blocks. In such cases, saccade inhibition is required for antisaccades but not for prosaccades. To more directly assess the role of the FEF in saccade inhibition and generation, a new paradigm was used in which inhibition was necessary on pro- and antisaccade trials. Participants looked in the direction indicated by a target ('<' or '>') that appeared in the left or right visual field. When the pointing direction and the location were congruent, prosaccades were executed; otherwise antisaccades were required. Saccadic latencies were measured in blocks without and with single pulse transcranial magnetic stimulation (TMS) to the right FEF or a right posterior control site. Results showed that antisaccades generated into the hemifield ipsilateral to the TMS were significantly delayed after TMS over the FEF, but not the posterior control site. This result is interpreted in terms of a modulation of saccade inhibition to the contralateral visual field due to disruption of processing in the FEF.     

Dynamics of directional selectivity in area 18 and PMLS of the cat

Visual latencies and temporal dynamics of area 18 and PMLS direction-selective complex cells were defined with a reverse correlation method. The method allowed us to analyze the time course of responses to motion steps, without confounding temporal integration effects. Several measures of response latency and direction tuning dynamics were quantified: optimal latency (OL), latency of first and last significant responses (FSR, LSR), the increase and decrease of direction sensitivity in time, and the change of direction tuning in time. FSR, OL and LSR values for PMLS and area 18 largely overlapped. The small differences in mean latencies (3-4 ms for FSR and OL and 11.9 ms for the LSR) were not statistically significant. All cells in area 18 and the vast majority of cells in PMLS showed no systematic changes in preferred direction (monophasic neurons). In PMLS 5 out of 41 cells showed a reversal of preferred direction after approximately 56 ms relative to their OL (biphasic neurons). Monophasic cells showed no systematic changes in direction tuning width during the interval from FSR to LSR. In both areas, development of direction sensitivity was significantly faster than return to the non-direction sensitive state, but no significant difference was found between the two areas. We conclude that, for the monophasic type of direction-selective complex cells, the dynamics of primary motion processing are highly comparable for area 18 and PMLS. This suggests that motion information is predominantly processed in parallel, presumably based on input from the fast conducting thalamocortical Y-pathway.     

A motion-sensitive area in ferret extrastriate visual cortex: an analysis in pigmented and albino animals

In search of the neuronal substrate for motion analysis in the ferret (Mustela putorius furo), we extracellularly recorded from extrastriate visual cortex in five pigmented and two albino ferrets under general anaesthesia and paralysis. Visual stimulation consisted of large area random dot patterns moving either on a circular path in the frontoparallel plane or expanding and contracting radially. Strongly direction-selective neurons were recorded in a circumscribed area in and just posterior to the suprasylvian sulcus, thus named by us the posterior suprasylvian area (area PSS). Altogether, we recorded 210 (90%) and 95 (72%) PSS neurons in pigmented and albino ferrets, respectively, that were direction selective. In these neurons responses during random dot pattern stimulation in the preferred direction were at least twice as strong than stimulation in the non-preferred direction. Response strength in preferred direction and tuning sharpness of PSS neurons in albinos were significantly reduced when compared to pigmented animals (median values: 34.1 versus 14.8 spikes/s and 142 versus 165 degrees for pigmented and albino ferrets, respectively). Inter-spike-intervals during visual stimulation were significantly shorter in pigmented (median 9 ms) than in albino PSS neurons (median 14 ms). Our data indicate that area PSS may play a crucial role in motion perception in the ferret.     

Functional differentiation of macaque visual temporal cortical neurons using a parametric action space

Neurons in the rostral superior temporal sulcus (STS) are responsive to displays of body movements. We employed a parametric action space to determine how similarities among actions are represented by visual temporal neurons and how form and motion information contributes to their responses. The stimulus space consisted of a stick-plus-point-light figure performing arm actions and their blends. Multidimensional scaling showed that the responses of temporal neurons represented the ordinal similarity between these actions. Further tests distinguished neurons responding equally strongly to static presentations and to actions ("snapshot" neurons), from those responding much less strongly to static presentations, but responding well when motion was present ("motion" neurons). The "motion" neurons were predominantly found in the upper bank/fundus of the STS, and "snapshot" neurons in the lower bank of the STS and inferior temporal convexity. Most "motion" neurons showed strong response modulation during the course of an action, thus responding to action kinematics. "Motion" neurons displayed a greater average selectivity for these simple arm actions than did "snapshot" neurons. We suggest that the "motion" neurons code for visual kinematics, whereas the "snapshot" neurons code for form/posture, and that both can contribute to action recognition, in agreement with computation models of action recognition.     

Temporal relation of population activity in visual areas MT/MST and in primary motor cortex during visually guided tracking movements

There is growing evidence that in primate cerebral cortex the areas along the 'dorsal pathway' are involved in the transformation of visual motion information towards a motor command. To pursue this cortical flow of information from visual motion areas to the motor cortex, single-cell activity was recorded from visual areas MT/MST (middle temporal area/medial superior temporal area) and from primary motor cortex (M1) while monkeys tracked moving targets with their right hand. Spike activity of 353 directionally tuned motor cortex cells was combined to a time-varying population vector, and similarly a time-resolved visual population vector was calculated from 252 MT/MST cells. Both population vectors code faithfully for the direction of the collinear motion of target and hand. For a given direction, the length of the population vectors varied over time during the performance of the task. The temporal evolution of both population responses reflects the different relationship between the early visual responses to the moving target and the directional motor command controlling the hand movement. The results indicate that during the visual tracking task visual and motor populations which code for similar directions of movement are co-activated with considerable temporal overlap. Despite this co-activation in both modalities, we failed to observe any significant synchronization between areas MT/MST and M1.     

Involvement of the ventral premotor cortex in controlling image motion of the hand during performance of a target-capturing task

The ventral premotor cortex (PMv) has been implicated in the visual guidance of movement. To examine whether neuronal activity in the PMv is involved in controlling the direction of motion of a visual image of the hand or the actual movement of the hand, we trained a monkey to capture a target that was presented on a video display using the same side of its hand as was displayed on the video display. We found that PMv neurons predominantly exhibited premovement activity that reflected the image motion to be controlled, rather than the physical motion of the hand. We also found that the activity of half of such direction-selective PMv neurons depended on which side (left versus right) of the video image of the hand was used to capture the target. Furthermore, this selectivity for a portion of the hand was not affected by changing the starting position of the hand movement. These findings suggest that PMv neurons play a crucial role in determining which part of the body moves in which direction, at least under conditions in which a visual image of a limb is used to guide limb movements.     

Contribution of GABAergic inhibition to receptive field structures of monkey inferior temporal neurons.

Receptive field (RF) structures of neurons in area TE of the monkey inferior temporal cortex were investigated under blockade of inhibition mediated by gamma-aminobutyric acid (GABA). Bicuculline methiodide, a GABA(A) receptor antagonist, was microiontophoretically administered to TE neurons. Blockade of inhibition enhanced responses to a particular range of visual stimuli not only at the RF center, but also at the periphery of or outside RFs where the stimuli originally evoked little or no response, enlarging the RFs. The strongest responses under normal and uninhibited conditions occurred at the RF center in most neurons. The largest increase in responses, reflecting the strongest inhibitory input, usually occurred at the RF center, but in some neurons it occurred in the periphery. A neuron had a silent region within its RF where some stimuli effective at adjacent locations could not elicit responses even under blockade of inhibition. We suggest that (i) afferent information to individual TE neurons originates from a wide retinotopic region beyond their normal RF; (ii) the afferent convergence is not necessarily complete throughout a RF; and (iii) GABAergic inhibition contributes to the generation of RF structures of TE neurons.     

Stimulus-dependent interaction between the visual areas 17 and 18 of the 2 hemispheres of the ferret (Mustela putorius)

To study how the visual areas of the 2 hemispheres interact in processing visual stimuli we have recorded local field potentials in the callosally connected parts of areas 17 and 18 of the ferret during the presentation of 3 kinds of stimuli: 2.5 degrees squares flashed for 50 ms randomly in the visual field (S1), 4 full-field gratings differing in orientation by 45 degrees and identical in the 2 hemifields (S2) and gratings as above but whose orientation and/or direction of motion differed by 90 degrees in the 2 hemifields (S3). The gratings remained stationary for 0.5 s and then moved in 1 of the 2 directions perpendicular to their orientation for 3 s. We compared the responses in baseline conditions with those obtained whereas the contralateral visual areas were inactivated by cooling. Cooling did not affect the responses to S1 but it modified those to S2 and to S3 generally increasing early components of the response while decreasing later components. These findings indicate that interhemispheric processing is restricted to visual stimuli which achieve spatial summation and that it involves complex inhibitory and facilitatory effects, possibly carried out by interhemispheric pathways of different conduction velocity.     

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.     

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.