Julio C. Martinez-Trujillo

Feature-Based Attention Increases the Selectivity of Population Responses in Primate Visual Cortex

BACKGROUND Attending to the spatial location or to nonspatial features of visual stimuli can modulate neuronal responses in primate visual cortex. The modulation by spatial attention changes the gain of sensory neurons and strengthens the representation of attended locations without changing neuronal selectivities such as directionality, i.e., the ratio of responses to preferred and anti-preferred directions of motion. Whether feature-based attention acts in a similar manner is unknown. RESULTS To clarify this issue, we recorded the responses of 135 direction-selective neurons in the middle temporal area (MT) of two macaques to an unattended moving random dot pattern (the distractor) positioned inside a neurons receptive field while the animals attended to a second moving pattern positioned in the opposite hemifield. Responses to different directions of the distractor were modulated by the same factor (approximately 12%) as long as the attended direction remained unchanged. On the other hand, systematically changing the attended direction from a neurons preferred to its anti-preferred direction caused a systematic change of the attentional modulation from an enhancement to a suppression, increasing directionality by about 20%. CONCLUSIONS The results show that (1) feature-based attention exerts a multiplicative modulation upon neuronal responses and that the strength of this modulation depends on the similarity between the attended feature and the cells preferred feature, in line with the feature-similarity gain model, and (2) at the level of the neuronal population, feature-based attention increases the selectivity for attended features by increasing the responses of neurons preferring this feature value while decreasing responses of neurons tuned to the opposite feature value.

Attentional modulation strength in cortical area MT depends on stimulus contrast.

The attentional modulation of sensory information processing in the visual system is the result of top-down influences, which can cause a multiplicative modulation of the firing rate of sensory neurons in extrastriate visual cortex, an effect reminiscent of the bottom-up effect of changes in stimulus contrast. This similarity could simply reflect the multiplicity of both effects. But, here we show that in direction-selective neurons in monkey visual cortical area MT, stimulus and attentional effects share a nonlinearity. These neurons show higher response gain for both contrast and attentional changes for intermediate contrast stimuli and smaller gain for low- and high-contrast stimuli. This finding suggests a close relationship between the neural encoding of stimulus contrast and the modulating effect of the behavioral relevance of stimuli.

Attending to visual motion

Visual motion analysis has focused on decomposing image sequences into their component features. There has been little success at re-combining those features into moving objects. Here a novel model of attentive visual motion processing is presented that addresses both decomposition of the signal into constituent features as well as the re-combination, or binding, of those features into wholes. A new feed-forward motion-processing pyramid is presented motivated by the neurobiology of primate motion processes. On this structure the Selective Tuning (ST) model for visual attention is demonstrated. There are three main contributions: (1) a new feed-forward motion processing hierarchy, the first to include a multi-level decomposition with local spatial derivatives of velocity: (2) examples of how ST operates on this hierarchy to attend to motion and to localize and label motion patterns: and (3) a new solution to the feature binding problem sufficient for grouping motion features into coherent object motion. Binding is accomplished using a top-down selection mechanism that does not depend on a single location-based saliency representation.

Sharp emergence of feature-selective sustained activity along the dorsal visual pathway

Sustained activity encoding visual working memory representations has been observed in several cortical areas of primates. Where along the visual pathways this activity emerges remains unknown. Here we show in macaques that sustained spiking activity encoding memorized visual motion directions is absent in direction-selective neurons in early visual area middle temporal (MT). However, it is robustly present immediately downstream, in multimodal association area medial superior temporal (MST), as well as and in the lateral prefrontal cortex (LPFC). This sharp emergence of sustained activity along the dorsal visual pathway suggests a functional boundary between early visual areas, which encode sensory inputs, and downstream association areas, which additionally encode mnemonic representations. Moreover, local field potential oscillations in MT encoded the memorized directions and, in the low frequencies, were phase-coherent with LPFC spikes. This suggests that LPFC sustained activity modulates synaptic activity in MT, a putative top-down mechanism by which memory signals influence stimulus processing in early visual cortex.

Frames of reference for eye-head gaze commands in primate supplementary eye fields.

The supplementary eye field (SEF) is a region within medial frontal cortex that integrates complex visuospatial information and controls eye-head gaze shifts. Here, we test if the SEF encodes desired gaze directions in a simple retinal (eye-centered) frame, such as the superior colliculus, or in some other, more complex frame. We electrically stimulated 55 SEF sites in two head-unrestrained monkeys to evoke 3D eye-head gaze shifts and then mathematically rotated these trajectories into various reference frames. Each stimulation site specified a specific spatial goal when plotted in its intrinsic frame. These intrinsic frames varied site by site, in a continuum from eye-, to head-, to space/body-centered coding schemes. This variety of coding schemes provides the SEF with a unique potential for implementing arbitrary reference frame transformations.

Attentional Filtering of Visual Information by Neuronal Ensembles in the Primate Lateral Prefrontal Cortex

The activity of neurons in the primate lateral prefrontal cortex (LPFC) is strongly modulated by visual attention. Such a modulation has mostly been documented by averaging the activity of independently recorded neurons over repeated experimental trials. However, in realistic settings, ensembles of simultaneously active LPFC neurons must generate attentional signals on a single-trial basis, despite the individual and correlated variability of neuronal responses. Whether, under these circumstances, the LPFC can reliably generate attentional signals is unclear. Here, we show that the simultaneous activity of neuronal ensembles in the primate LPFC can be reliably decoded to predict the allocation of attention on a single-trial basis. Decoding was sensitive to the noise correlation structure of the ensembles. Additionally, it was resilient to distractors, predictive of behavior, and stable over weeks. Thus, LPFC neuronal ensemble activity can reliably encode attention within behavioral time frames, despite the noisy and correlated nature of neuronal activity.

Prefrontal Neurons of Opposite Spatial Preference Display Distinct Target Selection Dynamics

Neurons in the primate dorsolateral prefrontal cortex (dlPFC) of one hemisphere are selective for the location of attended targets in both visual hemifields. Whether dlPFC neurons with selectivity for opposite hemifields directly compete with each other for target selection or instead play distinct roles during the allocation of attention remains unclear. We explored this issue by recording neuronal responses in the right dlPFC of two macaques while they allocated attention to a target in one hemifield and ignored a distracter on the opposite side. Forty-nine percent of the recorded neurons were target location selective. Neurons selective for contralateral targets (58%) systematically discriminated targets from distracters faster than neurons selective for ipsilateral targets (42%). Additionally, during trials in which sensory stimulation remained the same but both stimuli were task irrelevant and animals were required to detect a change in the color of a fixation spot, contralateral neurons still reliably discriminated the putative target from the distracter, whereas ipsilateral neurons did not. The latter result indicates that target-distracter discrimination by contralateral neurons could occur independently of discrimination by ipsilateral cells; thus, the two cell types may represent two different components of the prefrontal circuitry underlying the allocation of attention to targets in the presence of distracters. Moreover, the response of both contralateral and ipsilateral neurons to a single target was substantially reduced by the presence of a distracter in the contralateral hemifield. This result suggests that the presence of the distracter triggered inhibitory interactions within the dlPFC circuitry that suppressed responses to the attended target.

Sustained Activity Encoding Working Memories: Not Fully Distributed

Working memory (WM) is the ability to remember and manipulate information for short time intervals. Recent studies have proposed that sustained firing encoding the contents of WM is ubiquitous across cortical neurons. We review here the collective evidence supporting this claim. A variety of studies report that neurons in prefrontal, parietal, and inferotemporal association cortices show robust sustained activity encoding the location and features of memoranda during WM tasks. However, reports of WM-related sustained activity in early sensory areas are rare, and typically lack stimulus specificity. We propose that robust sustained activity that can support WM coding arises as a property of association cortices downstream from the early stages of sensory processing.

Electrical stimulation of the frontal eye fields in the head-free macaque evokes kinematically normal 3D gaze shifts.

The frontal eye field (FEF) is a region of the primate prefrontal cortex that is central to eye-movement generation and target selection. It has been shown that neurons in this area encode commands for saccadic eye movements. Furthermore, it has been suggested that the FEF may be involved in the generation of gaze commands for the eye and the head. To test this suggestion, we systematically stimulated (with pulses of 300 Hz frequency, 200 ms duration, 30-100 μA intensity) the FEF of two macaques, with the head unrestrained, while recording three-dimensional (3D) eye and head rotations. In a total of 95 sites, the stimulation consistently elicited gaze-orienting movements ranging in amplitude from 2 to 172°, directed contralateral to the stimulation site, and with variable vertical components. These movements were typically a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between the stimulation-evoked movements and gaze shifts voluntarily made by the animal. The kinematics of the stimulation-evoked movements (i.e., their spatiotemporal properties, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were very similar to those of natural gaze shifts. Moreover, they obeyed the same 3D constraints as the natural gaze shifts (i.e., modified Listings law for eye-in-head movements). As in natural gaze shifts, saccade and vestibuloocular reflex torsion during stimulation-evoked movements were coordinated so that at the end of the head movement the eye-in-head ended up in Listings plane. In summary, movements evoked by stimulation of the FEF closely resembled those of naturally occurring eye-head gaze shifts. Thus we conclude that the FEF explicitly encodes gaze commands and that the kinematic aspects of eye-head coordination are likely specified by downstream mechanisms.

Selectivity for speed gradients in human area MT/V5.

Cortical area MT/V5 in the human occipito-temporal cortex is activated by visual motion. In this study, we use functional imaging to demonstrate that a subregion of MT/V5 is more strongly activated by unidirectional motion with speed gradients than by other motion patterns. Our results suggest that like the monkey homolog middle temporal area (MT), human MT/V5 contains neurons selective for the processing of speed gradients. Such neurons may constitute an intermediate stage of processing between neurons selective for the average speed of unidirectional motion and neurons selective for different combinations of speed gradient and different motion directions such as expanding optical flow patterns.