Visual stimulus-driven functional organization of macaque prefrontal cortex.

The extent to which the major subdivisions of prefrontal cortex (PFC) can be functionally partitioned is unclear. In approaching the question, it is often assumed that the organization is task dependent. Here we use fMRI to show that PFC can respond in a task-independent way, and we leverage these responses to uncover a stimulus-driven functional organization. The results were generated by mapping the relative location of responses to faces, bodies, scenes, disparity, color, and eccentricity in four passively fixating macaques. The results control for individual differences in functional architecture and provide the first account of a systematic visual stimulus-driven functional organization across PFC. Responses were focused in dorsolateral PFC (DLPFC), in the ventral prearcuate region; and in ventrolateral PFC (VLPFC), extending into orbital PFC. Face patches were in the VLPFC focus and were characterized by a striking lack of response to non-face stimuli rather than an especially strong response to faces. Color-biased regions were near but distinct from face patches. One scene-biased region was consistently localized with different contrasts and overlapped the disparity-biased region to define the DLPFC focus. All visually responsive regions showed a peripheral visual-field bias. These results uncover an organizational scheme that presumably constrains the flow of information about different visual modalities into PFC.

Representation of Perceptual Color Space in Macaque Posterior Inferior Temporal Cortex (the V4 Complex).

The lateral geniculate nucleus is thought to represent color using two populations of cone-opponent neurons [L vs M; S vs (L + M)], which establish the cardinal directions in color space (reddish vs cyan; lavender vs lime). How is this representation transformed to bring about color perception? Prior work implicates populations of glob cells in posterior inferior temporal cortex (PIT; the V4 complex), but the correspondence between the neural representation of color in PIT/V4 complex and the organization of perceptual color space is unclear. We compared color-tuning data for populations of glob cells and interglob cells to predictions obtained using models that varied in the color-tuning narrowness of the cells, and the color preference distribution across the populations. Glob cells were best accounted for by simulated neurons that have nonlinear (narrow) tuning and, as a population, represent a color space designed to be perceptually uniform (CIELUV). Multidimensional scaling and representational similarity analyses showed that the color space representations in both glob and interglob populations were correlated with the organization of CIELUV space, but glob cells showed a stronger correlation. Hue could be classified invariant to luminance with high accuracy given glob responses and above-chance accuracy given interglob responses. Luminance could be read out invariant to changes in hue in both populations, but interglob cells tended to prefer stimuli having luminance contrast, regardless of hue, whereas glob cells typically retained hue tuning as luminance contrast was modulated. The combined luminance/hue sensitivity of glob cells is predicted for neurons that can distinguish two colors of the same hue at different luminance levels (orange/brown).

Functional architecture for disparity in macaque inferior temporal cortex and its relationship to the architecture for faces, color, scenes, and visual field.

Binocular disparity is a powerful depth cue for object perception. The computations for object vision culminate in inferior temporal cortex (IT), but the functional organization for disparity in IT is unknown. Here we addressed this question by measuring fMRI responses in alert monkeys to stimuli that appeared in front of (near), behind (far), or at the fixation plane. We discovered three regions that showed preferential responses for near and far stimuli, relative to zero-disparity stimuli at the fixation plane. These "near/far" disparity-biased regions were located within dorsal IT, as predicted by microelectrode studies, and on the posterior inferotemporal gyrus. In a second analysis, we instead compared responses to near stimuli with responses to far stimuli and discovered a separate network of "near" disparity-biased regions that extended along the crest of the superior temporal sulcus. We also measured in the same animals fMRI responses to faces, scenes, color, and checkerboard annuli at different visual field eccentricities. Disparity-biased regions defined in either analysis did not show a color bias, suggesting that disparity and color contribute to different computations within IT. Scene-biased regions responded preferentially to near and far stimuli (compared with stimuli without disparity) and had a peripheral visual field bias, whereas face patches had a marked near bias and a central visual field bias. These results support the idea that IT is organized by a coarse eccentricity map, and show that disparity likely contributes to computations associated with both central (face processing) and peripheral (scene processing) visual field biases, but likely does not contribute much to computations within IT that are implicated in processing color.

Role of medio-dorsal frontal and posterior parietal neurons during auditory detection performance in rats.

To further characterize the role of frontal and parietal cortices in rat cognition, we recorded action potentials simultaneously from multiple sites in the medio-dorsal frontal cortex and posterior parietal cortex of rats while they performed a two-choice auditory detection task. We quantified neural correlates of task performance, including response movements, perception of a target tone, and the differentiation between stimuli with distinct features (different pitches or durations). A minority of units--15% in frontal cortex, 23% in parietal cortex--significantly distinguished hit trials (successful detections, response movement to the right) from correct rejection trials (correct leftward response to the absence of the target tone). Estimating the contribution of movement-related activity to these responses suggested that more than half of these units were likely signaling correct perception of the auditory target, rather than merely movement direction. In addition, we found a smaller and mostly not overlapping population of units that differentiated stimuli based on task-irrelevant details. The detection-related spiking responses we observed suggest that correlates of perception in the rat are sparsely represented among neurons in the rat's frontal-parietal network, without being concentrated preferentially in frontal or parietal areas.

Color-detection thresholds in rhesus macaque monkeys and humans.

Macaque monkeys are a model of human color vision. To facilitate linking physiology in monkeys with psychophysics in humans, we directly compared color-detection thresholds in humans and rhesus monkeys. Colors were defined by an equiluminant plane of cone-opponent color space. All subjects were tested on an identical apparatus with a four-alternative forced-choice task. Targets were 2° square, centered 2° from fixation, embedded in luminance noise. Across all subjects, the change in detection thresholds from initial testing to plateau performance ("learning") was similar for +L − M (red) colors and +M − L (bluish-green) colors. But the extent of learning was higher for +S (lavender) than for −S (yellow-lime); moreover, at plateau performance, the cone contrast at the detection threshold was higher for +S than for −S. These asymmetries may reflect differences in retinal circuitry for S-ON and S-OFF. At plateau performance, the two species also had similar detection thresholds for all colors, although monkeys had shorter reaction times than humans and slightly lower thresholds for colors that modulated L/M cones. We discuss whether these observations, together with previous work showing that monkeys have lower spatial acuity than humans, could be accounted for by selective pressures driving higher chromatic sensitivity at the cost of spatial acuity amongst monkeys, specifically for the more recently evolved L − M mechanism.

Prestimulus frontal-parietal coherence predicts auditory detection performance in rats.

Electrophysiology in primates has implicated long-range neural coherence as a potential mechanism for enhancing sensory detection. To test whether local synchronization and long-range neural coherence support detection performance in rats, we recorded local field potentials (LFPs) in frontal and parietal cortex while rats performed an auditory detection task. We observed significantly elevated power at multiple low frequencies (<15 Hz) preceding the target beep when the animal failed to respond to the signal (misses), in both frontal and parietal cortex. In terms of long-range coherence, we observed significantly more frontal-parietal coherence in the beta band (15-30 Hz) before the signal on misses compared with hits. This effect persisted after regressing away linear trends in the coherence values during a session, showing that the excess frontal-parietal beta coherence prior to misses cannot be explained by slow motivational changes during a session. In addition, a trend toward higher low-frequency (<15 Hz) coherence prior to miss trials compared with hits became highly significant when we rereferenced the LFPs to the mean voltage on each recording array, suggesting that the results are specific to our frontal and parietal areas. These results do not support a role for long-range frontal-parietal coherence or local synchronization in facilitating the detection of external stimuli. Rather, they extend to long-range frontal-parietal coherence previous findings that correlate local synchronization of low-frequency (<15 Hz) oscillations with inattention to external stimuli and synchronization of beta rhythms (15-30 Hz) with voluntary or involuntary prolongation of the current cognitive or motor state.