Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems.

The neural bases of attention, a set of neural processes that promote behavioral selection, is a subject of intense investigation. In humans, rewarded cues influence attention, even when those cues are irrelevant to the current task. Because the amygdala plays a role in reward processing, and the activity of amygdala neurons has been linked to spatial attention, we reasoned that the amygdala may be essential for attending to rewarded images. To test this possibility, we used an attentional capture task, which provides a quantitative measure of attentional bias. Specifically, we compared reaction times (RTs) of adult male rhesus monkeys with bilateral amygdala lesions and unoperated controls as they made a saccade away from a high- or low-value rewarded image to a peripheral target. We predicted that: (1) RTs will be longer for high- compared with low-value images, revealing attentional capture by rewarded stimuli; and (2) relative to controls, monkeys with amygdala lesions would exhibit shorter RT for high-value images. For comparison, we assessed the same groups of monkeys for attentional capture by images of predators and conspecifics, categories thought to have innate biological value. In performing the attentional capture task, all monkeys were slowed more by high-value relative to low-value rewarded images. Contrary to our prediction, amygdala lesions failed to disrupt this effect. When presented with images of predators and conspecifics, however, monkeys with amygdala lesions showed significantly diminished attentional capture relative to controls. Thus, separate neural pathways are responsible for allocating attention to stimuli with learned versus innate value.SIGNIFICANCE STATEMENT Valuable objects attract attention. The amygdala is known to contribute to reward processing and the encoding of object reward value. We therefore examined whether the amygdala is necessary for allocating attention to rewarded objects. For comparison, we assessed the amygdala's contribution to attending to objects with innate biological value: predators and conspecifics. We found that the macaque amygdala is necessary for directing attention to images with innate biological value, but not for directing attention to recently learned reward-predictive images. These findings indicate that the amygdala makes selective contributions to attending to valuable objects. The data are relevant to mental health disorders, such as social anxiety disorders and small animal phobias, that arise from biased attention to select categories of objects.

Gustatory responses in macaque monkeys revealed with fMRI: Comments on taste, taste preference, and internal state.

Studies of the neural mechanisms underlying value-based decision making typically employ food or fluid rewards to motivate subjects to perform cognitive tasks. Rewards are often treated as interchangeable, but it is well known that the specific tastes of foods and fluids and the values associated with their taste sensations influence choices and contribute to overall levels of food consumption. Accordingly, we characterized the gustatory system in three macaque monkeys (Macaca mulatta) and examined whether gustatory responses were modulated by preferences and hydration status. To identify taste-responsive cortex, we delivered small quantities (0.1 ml) of sucrose (sweet), citric acid (sour), or distilled water in random order without any predictive cues while scanning monkeys using event-related fMRI. Neural effects were evaluated by using each session in each monkey as a data point in a second-level analysis. By contrasting BOLD responses to sweet and sour tastes with those from distilled water in a group level analysis, we identified taste responses in primary gustatory cortex area G, an adjacent portion of the anterior insular cortex, and prefrontal cortex area 12o. Choice tests administered outside the scanner revealed that all three monkeys strongly preferred sucrose to citric acid or water. BOLD responses in the ventral striatum, ventral pallidum, and amygdala reflected monkeys' preferences, with greater BOLD responses to sucrose than citric acid. Finally, we examined the influence of hydration level by contrasting BOLD responses to receipt of fluids when monkeys were thirsty and after ad libitum water consumption. BOLD responses in area G and area 12o in the left hemisphere were greater following full hydration. By contrast, BOLD responses in portions of medial frontal cortex were reduced after ad libitum water consumption. These findings highlight brain regions involved in representing taste, taste preference and internal state.

Learned Value Shapes Responses to Objects in Frontal and Ventral Stream Networks in Macaque Monkeys.

We have an incomplete picture of how the brain links object representations to reward value, and how this information is stored and later retrieved. The orbitofrontal cortex (OFC), medial frontal cortex (MFC), and ventrolateral prefrontal cortex (VLPFC), together with the amygdala, are thought to play key roles in these processes. There is an apparent discrepancy, however, regarding frontal areas thought to encode value in macaque monkeys versus humans. To address this issue, we used fMRI in macaque monkeys to localize brain areas encoding recently learned image values. Each week, monkeys learned to associate images of novel objects with a high or low probability of water reward. Areas responding to the value of recently learned reward-predictive images included MFC area 10 m/32, VLPFC area 12, and inferior temporal visual cortex (IT). The amygdala and OFC, each thought to be involved in value encoding, showed little such effect. Instead, these 2 areas primarily responded to visual stimulation and reward receipt, respectively. Strong image value encoding in monkey MFC compared with OFC is surprising, but agrees with results from human imaging studies. Our findings demonstrate the importance of VLPFC, MFC, and IT in representing the values of recently learned visual images.

Cortical and subcortical connections of V1 and V2 in early postnatal macaque monkeys.

Connections of primary (V1) and secondary (V2) visual areas were revealed in macaque monkeys ranging in age from 2 to 16 weeks by injecting small amounts of cholera toxin subunit B (CTB). Cortex was flattened and cut parallel to the surface to reveal injection sites, patterns of labeled cells, and patterns of cytochrome oxidase (CO) staining. Projections from the lateral geniculate nucleus and pulvinar to V1 were present at 4 weeks of age, as were pulvinar projections to thin and thick CO stripes in V2. Injections into V1 in 4- and 8-week-old monkeys labeled neurons in V2, V3, middle temporal area (MT), and dorsolateral area (DL)/V4. Within V1 and V2, labeled neurons were densely distributed around the injection sites, but formed patches at distances away from injection sites. Injections into V2 labeled neurons in V1, V3, DL/V4, and MT of monkeys 2-, 4-, and 8-weeks of age. Injections in thin stripes of V2 preferentially labeled neurons in other V2 thin stripes and neurons in the CO blob regions of V1. A likely thick stripe injection in V2 at 4 weeks of age labeled neurons around blobs. Most labeled neurons in V1 were in superficial cortical layers after V2 injections, and in deep layers of other areas. Although these features of adult V1 and V2 connectivity were in place as early as 2 postnatal weeks, labeled cells in V1 and V2 became more restricted to preferred CO compartments after 2 weeks of age.

Orientation and Direction-of-Motion Response in the Middle Temporal Visual Area (MT) of New World Owl Monkeys as Revealed by Intrinsic-Signal Optical Imaging.

Intrinsic-signal optical imaging was used to evaluate relationships of domains of neurons in middle temporal visual area (MT) selective for stimulus orientation and direction-of-motion. Maps of activation were elicited in MT of owl monkeys by gratings drifting back-and-forth, flashed stationary gratings and unidirectionally drifting fields of random dots. Drifting gratings, typically used to reveal orientation preference domains, contain a motion component that may be represented in MT. Consequently, this stimulus could activate groups of cells responsive to the motion of the grating, its orientation or a combination of both. Domains elicited from either moving or static gratings were remarkably similar, indicating that these groups of cells are responding to orientation, although they may also encode information about motion. To assess the relationship between domains defined by drifting oriented gratings and those responsive to direction-of-motion, the response to drifting fields of random dots was measured within domains defined from thresholded maps of activation elicited by the drifting gratings. The optical response elicited by drifting fields of random dots was maximal in a direction orthogonal to the map of orientation preference. Thus, neurons in domains selective for stimulus orientation are also selective for motion orthogonal to the preferred stimulus orientation.

The organization of orientation-selective, luminance-change and binocular- preference domains in the second (V2) and third (V3) visual areas of New World owl monkeys as revealed by intrinsic signal optical imaging.

Optical imaging was used to map patterns of visually evoked activation in the second (V2) and third (V3) visual areas of owl monkeys. Modular patterns of activation were produced in response to stimulation with oriented gratings, binocular versus monocular stimulation, and stimuli containing wide-field luminance changes. In V2, luminance-change domains tended to lie between domains selective for orientation. Regions preferentially activated by binocular stimulation co-registered with orientation-selective domains. Co-alignment of images with cytochrome oxidase (CO)-processed sections revealed functional correlates of 2 types of CO-dense regions in V2. Orientation-responsive domains and binocular domains were correlated with the locations of CO-thick stripes, and luminance-change domains were correlated with the locations of CO-thin stripes. In V3, orientation preference, luminance-change, and binocular preference domains were observed, but were more irregularly arranged than those in V2. Our data suggest that in owl monkey V2, consistent with that in macaque monkeys, modules for processing contours and binocularity exist in one type of compartment and that modules related to processing-surface features exist within a separate type of compartment.

Cortical connections of the middle temporal and the middle temporal crescent visual areas in prosimian galagos (Otolemur garnetti).

While considerable progress has been made in understanding the organization of visual cortex in monkeys, less is known about the visual systems of prosimians. The middle temporal visual area (MT), an area involved in motion perception, is common to all primates. We placed injections of tracers in MT and just caudal to MT in cortex expected to be the MT crescent (MTc), an area previously identified in monkeys but not in prosimians. We analyzed the patterns of projections in sections of the flattened cortex and used sections stained for cytochrome oxidase (CO) and myelin to identify the borders of MT, MTc, middle superior temporal (MST), superior temporal sulcus (FST), and V1 and V2 and to identify possible subdivisions of these areas. As in owl monkeys, MTc is a belt around most of MT that consists of a single row of CO-dense patches in a CO-light surround. Injections placed in MT revealed connections with V1, V2, V3, FST, MST, MTc, dorsomedial, dorsolateral (DL), posterior parietal cortex, and inferotemporal (IT) cortex. Injections localized to MTc displayed a slightly different pattern of connections with more involvement of DL and IT cortex, though other aspects, including patchy connections with V1 and V2, were similar to MT connections. The results indicate that prosimian galagos have an MT area with connection patterns that are similar to those in New and Old World monkeys. The MTc, initially described in owl monkeys, is present in galagos and is likely to be a common component of primate visual cortex.

Intrinsic-signal optical imaging reveals cryptic ocular dominance columns in primary visual cortex of New World owl monkeys.

A significant concept in neuroscience is that sensory areas of the neocortex have evolved the remarkable ability to represent a number of stimulus features within the confines of a global map of the sensory periphery. Modularity, the term often used to describe the inhomogeneous nature of the neocortex, is without a doubt an important organizational principle of early sensory areas, such as the primary visual cortex (V1). Ocular dominance columns, one type of module in V1, are found in many primate species as well as in carnivores. Yet, their variable presence in some New World monkey species and complete absence in other species has been enigmatic. Here, we demonstrate that optical imaging reveals the presence of ocular dominance columns in the superficial layers of V1 of owl monkeys (Aotus trivirgatus), even though the geniculate inputs related to each eye are highly overlapping in layer 4. The ocular dominance columns in owl monkeys revealed by optical imaging are circular in appearance. The distance between left eye centers and right eye centers is approximately 650 mum. We find no relationship between ocular dominance centers and other modular organizational features such as orientation pinwheels or the centers of the cytochrome oxidase blobs. These results are significant because they suggest that functional columns may exist in the absence of obvious differences in the distributions of activating inputs and ocular dominance columns may be more widely distributed across mammalian taxa than commonly suggested.

Peripheral variability and central constancy in mammalian visual system evolution.

Neural systems are necessarily the adaptive products of natural selection, but a neural system, dedicated to any particular function in a complex brain, may be composed of components that covary with functionally unrelated systems, owing to constraints beyond immediate functional requirements. Some studies support a modular or mosaic organization of the brain, whereas others emphasize coordination and covariation. To contrast these views, we have analysed the retina, striate cortex (V1) and extrastriate cortex (V2, V3, MT, etc.) in 30 mammals, examining the area of the neocortex and individual neocortical areas and the relative numbers of rods and cones. Controlling for brain size and species relatedness, the sizes of visual cortical areas (striate, extrastriate) within the brains of nocturnal and diurnal mammals are not statistically different from one another. The relative sizes of all cortical areas, visual, somatosensory and auditory, are best predicted by the total size of the neocortex. In the sensory periphery, the retina is clearly specialized for niche. New data on rod and cone numbers in various New World primates confirm that rod and cone complements of the retina vary substantially between nocturnal and diurnal species. Although peripheral specializations or receptor surfaces may be highly susceptible to niche-specific selection pressures, the areal divisions of the cerebral cortex are considerably more conservative.

Optical imaging of visually evoked responses in the middle temporal area after deactivation of primary visual cortex in adult primates.

The middle temporal area (MT) is a visual area in primates with direct and indirect inputs from the primary visual cortex (V1), a role in visual motion perception, and a suggested role in "blindsight." When V1 is deactivated, some studies report continued activation of MT neurons, which has been attributed to an indirect pathway to MT from the superior colliculus. Here we used muscimol to deactivate V1 while optically imaging visually evoked activity in MT in two primates, owl monkeys and galagos, where MT is exposed on the brain surface. The partial loss of V1 inputs abolished all or nearly all evoked activity in the retinotopically matched part of MT. Low levels of activation that persisted in portions of MT that were unstimulated or retinotopically congruent with the blocked portion of V1 appeared to reflect the spread of activity from stimulated to unstimulated parts of MT. Thus, a significant pathway based on the superior colliculus was not demonstrated.

Optical imaging of visually evoked responses in prosimian primates reveals conserved features of the middle temporal visual area.

Optical imaging of intrinsic cortical responses to visual stimuli was used to characterize the organization of the middle temporal visual area (MT) of a prosimian primate, the bush baby (Otolemur garnetti). Stimulation with moving gratings revealed a patchwork of oval-like domains in MT. These orientation domains could, in turn, be subdivided into zones selective to directional movements that were mainly orthogonal to the preferred orientation. Similar, but not identical, zones were activated by movements of random dots in the preferred direction. Orientation domains shifted in preference systematically either around a center to form pinwheels or as gradual linear shifts. Stimuli presented in different portions of the visual field demonstrated a global representation of visual space in MT. As optical imaging has revealed similar features in MT of New World monkeys, MT appears to have retained these basic features of organization for at least the 60 million years since the divergence of prosimian and simian primates.