No abstract

We perceive real-world objects as three-dimensional (3D), yet it is unknown which brain area underlies our ability to perceive objects in this way. The macaque inferotemporal (IT) cortex contains neurons that respond selectively to 3D structures defined by binocular disparity. To examine the causal role of IT in the categorization of 3D structures, we electrically stimulated clusters of IT neurons with a similar 3D-structure preference while monkeys performed a 3D-structure categorization task. Microstimulation of 3D-structure-selective IT clusters caused monkeys to choose the preferred structure of the 3D-structure-selective neurons considerably more often. Microstimulation in IT also accelerated the monkeys' choice for the preferred structure, while delaying choices corresponding to the nonpreferred structure of a given site. These findings reveal that 3D-structure-selective neurons in IT contribute to the categorization of 3D objects.

Attention is believed to enhance perception by altering the correlations between pairs of neurons. How attention changes neuronal correlations is unknown. Using multi-electrodes in primate visual cortex, we measured spike-count correlations when single or multiple stimuli were presented, and stimuli were attended or unattended. When stimuli were unattended, adding a suppressive, non-preferred, stimulus beside a preferred stimulus increased spike-count correlations between pairs of similarly-tuned neurons, but decreased spike-count correlations between pairs of oppositely-tuned neurons. These changes are explained by a stochastic normalization model containing populations of oppositely-tuned, mutually-suppressive neurons. Importantly, this model also explains why attention decreased (attend preferred stimulus) or increased (attend non-preferred stimulus) correlations: as an indirect consequence of attention-related changes in the inputs to normalization mechanisms. Our findings link normalization mechanisms to correlated neuronal activity and attention, showing that normalization mechanisms shape response correlations and that these correlations change when attention biases normalization mechanisms.

The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-microstimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams.

One of the fundamental goals of neuroscience is to understand how perception arises from the activity of neurons in the brain. Stereopsis is a type of three-dimensional (3D) perception that relies on two slightly different projections of the world onto the retinas of the two eyes, i.e., binocular disparity. Neurons selective for curved surfaces defined by binocular disparity may contribute to the perception of an object's 3D structure. Such neurons have been observed in both the anterior lower bank of the superior temporal sulcus (TEs, part of the inferior temporal cortex [IT]) and the anterior intraparietal area (AIP). However, the specific contributions of IT and AIP to depth perception remain unknown. We simultaneously recorded multiunit activity in IT and AIP while monkeys discriminated between concave and convex 3D shapes. We observed a correlation between the neural activity and behavioral choice that arose early and during perceptual decision formation in IT but later and after perceptual decision formation in AIP. These results suggest a role for IT, but not AIP, in 3D shape discrimination. Furthermore, the results demonstrate that similar neuronal stimulus selectivities in two areas do not imply a similar function.

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 eccentricitymap,andshowthatdisparitylikelycontributestocomputationsassociatedwithbothcentral(faceprocessing)andperipheral(scene processing) visual field biases, but likely does not contribute much to computations within IT that are implicated in processing color.

Verhoef B, Vogels R, Janssen P. Synchronization between the end stages of the dorsal and the ventral visual stream. J Neurophysiol 105: 2030 -2042, 2011. First published February 16, 2011 doi:10.1152/jn.00924.2010.-The end stage areas of the ventral (IT) and the dorsal (AIP) visual streams encode the shape of disparitydefined three-dimensional (3D) surfaces. Recent anatomical tracer studies have found direct reciprocal connections between the 3D-shape selective areas in IT and AIP. Whether these anatomical connections are used to facilitate 3D-shape perception is still unknown. We simultaneously recorded multi-unit activity (MUA) and local field potentials in IT and AIP while monkeys discriminated between concave and convex 3D shapes and measured the degree to which the activity in IT and AIP synchronized during the task. We observed strong beta-band synchronization between IT and AIP preceding stimulus onset that decreased shortly after stimulus onset and became modulated by stereo-signal strength and stimulus contrast during the later portion of the stimulus period. The beta-coherence modulation was unrelated to task-difficulty, regionally specific, and dependent on the MUA selectivity of the pairs of sites under study. The beta-spikefield coherence in AIP predicted the upcoming choice of the monkey. Several convergent lines of evidence suggested AIP as the primary source of the AIP-IT synchronized activity. The synchronized beta activity seemed to occur during perceptual anticipation and when the system has stabilized to a particular perceptual state but not during active visual processing. Our findings demonstrate for the first time that synchronized activity exists between the end stages of the dorsal and ventral stream during 3D-shape discrimination. three-dimensional shape perception; synchronization TO UNDERSTAND THE FUNCTIONING of brain networks, one must know the properties of its constituting elements and the interconnections between them. Traditional neuroscience has mainly focused on the functional properties of brain elements (e.g., feature tuning of neurons or the functional role of brain regions). However, recently there has been an increased interest in the brain's "connectome" (Sporns et al. 2005), i.e., the neural connections at the micro-, meso-, and macroscale.

Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround.DOI: http://dx.doi.org/10.7554/eLife.17256.001