Ryan E. B. Mruczek

Probabilistic Maps of Visual Topography in Human Cortex

The human visual system contains an array of topographically organized regions. Identifying these regions in individual subjects is a powerful approach to group-level statistical analysis, but this is not always feasible. We addressed this limitation by generating probabilistic maps of visual topographic areas in 2 standardized spaces suitable for use with adult human brains. Using standard fMRI paradigms, we identified 25 topographic maps in a large population of individual subjects (N = 53) and transformed them into either a surface- or volume-based standardized space. Here, we provide a quantitative characterization of the inter-subject variability within and across visual regions, including the likelihood that a given point would be classified as a part of any region (full probability map) and the most probable region for any given point (maximum probability map). By evaluating the topographic organization across the whole of visual cortex, we provide new information about the organization of individual visual field maps and large-scale biases in visual field coverage. Finally, we validate each atlas for use with independent subjects. Overall, the probabilistic atlases quantify the variability of topographic representations in human cortex and provide a useful reference for comparing data across studies that can be transformed into these standard spaces.

Functional organization of human posterior parietal cortex: grasping- and reaching-related activations relative to topographically organized cortex

The act of reaching to grasp an object requires the coordination between transporting the arm and shaping the hand. Neurophysiological, neuroimaging, neuroanatomic, and neuropsychological studies in macaque monkeys and humans suggest that the neural networks underlying grasping and reaching acts are at least partially separable within the posterior parietal cortex (PPC). To better understand how these neural networks have evolved in primates, we characterized the relationship between grasping- and reaching-related responses and topographically organized areas of the human intraparietal sulcus (IPS) using functional MRI. Grasping-specific activation was localized to the left anterior IPS, partially overlapping with the most anterior topographic regions and extending into the postcentral sulcus. Reaching-specific activation was localized to the left precuneus and superior parietal lobule, partially overlapping with the medial aspects of the more posterior topographic regions. Although the majority of activity within the topographic regions of the IPS was nonspecific with respect to movement type, we found evidence for a functional gradient of specificity for reaching and grasping movements spanning posterior-medial to anterior-lateral PPC. In contrast to the macaque monkey, grasp- and reach-specific activations were largely located outside of the human IPS.

The representation of tool and non-tool object information in the human intraparietal sulcus

Humans have an amazing ability to quickly and efficiently recognize and interact with visual objects in their environment. The underlying neural processes supporting this ability have been mainly explored in the ventral visual stream. However, the dorsal stream has been proposed to play a critical role in guiding object-directed actions. This hypothesis is supported by recent neuroimaging studies that have identified object-selective and tool-related activity in human parietal cortex. In the present study, we sought to delineate tool-related information in the anterior portions of the human intraparietal sulcus (IPS) and relate it to recently identified motor-defined and topographic regions of interest (ROIs) using functional MRI in individual subjects. Consistent with previous reports, viewing pictures of tools compared with pictures of animals led to a higher blood oxygenation level-dependent (BOLD) response in the left anterior IPS. For every subject, this activation was located lateral, anterior, and inferior to topographic area IPS5 and lateral and inferior to a motor-defined human parietal grasp region (hPGR). In a separate experiment, subjects viewed pictures of tools, animals, graspable (non-tool) objects, and scrambled objects. An ROI-based time-course analysis showed that tools evoked a stronger BOLD response than animals throughout topographic regions of the left IPS. Additionally, graspable objects evoked stronger responses than animals, equal to responses to tools, in posterior regions and weaker responses than tools, equal to responses to animals, in anterior regions. Thus the left anterior tool-specific region may integrate visual information encoding graspable features of objects from more posterior portions of the IPS with experiential knowledge of object use and function to guide actions.

Effects of Familiarity on Neural Activity in Monkey Inferior Temporal Lobe

Long-term familiarity facilitates recognition of visual stimuli. To better understand the neural basis for this effect, we measured the local field potential (LFP) and multiunit spiking activity (MUA) from the inferior temporal (IT) lobe of behaving monkeys in response to novel and familiar images. In general, familiar images evoked larger amplitude LFPs whereas MUA responses were greater for novel images. Familiarity effects were attenuated by image rotations in the picture plane of 45 degrees. Decreasing image contrast led to more pronounced decreases in LFP response magnitude for novel, compared with familiar images, and resulted in more selective MUA response profiles for familiar images. The shape of individual LFP traces could be used for stimulus classification, and classification performance was better for the familiar image category. Recording the visual and auditory evoked LFP at multiple depths showed significant alterations in LFP morphology with distance changes of 2 mm. In summary, IT cortex shows local processing differences for familiar and novel images at a time scale and in a manner consistent with the observed behavioral advantage for classifying familiar images and rapidly detecting novel stimuli.

Distractor familiarity leads to more efficient visual search for complex stimuli.

Previous reports suggest that distractor familiarity plays an important role in determining visual search efficiency. However, the specific tasks used in those studies limit the extension of their findings to real-world situations and everyday images. In the present study, subjects engaged in a prolonged period of search experience as a control of their level of familiarity with a large set of target and distractor images. Reaction times and search slopes decreased dramatically over this period, especially for trials with a large target eccentricity and many distractors. Following extended practice, search among familiar distractors was more efficient than search among unfamiliar distractors. Furthermore, we found that familiar targets were located more efficiently than unfamiliar targets and that subjects were faster at locating targets that they had experienced in the majority of the search trials. These results show that prolonged visual experience facilitates processing of both target and distractor items during search.

Context Familiarity Enhances Target Processing by Inferior Temporal Cortex Neurons

Experience-dependent changes in the response properties of ventral visual stream neurons are thought to underlie our ability to rapidly and efficiently recognize visual objects. How these neural changes are related to efficient visual processing during natural vision remains unclear. Here, we demonstrate a neurophysiological correlate of efficient visual search through highly familiar object arrays. Humans and monkeys are faster at locating the same target when it is surrounded by familiar compared with unfamiliar distractors. We show that this behavioral enhancement is driven by an increased sensitivity of target-selective neurons in inferior temporal cortex. This results from an increased “signal” for target representations and decreased “noise” from neighboring familiar distractors. These data highlight the dynamic properties of the inferior temporal cortex neurons and add to a growing body of evidence demonstrating how experience shapes neural processing in the ventral visual stream.

Widespread correlation patterns of fMRI signal across visual cortex reflect eccentricity organization

The human visual system can be divided into over two-dozen distinct areas, each of which contains a topographic map of the visual field. A fundamental question in vision neuroscience is how the visual system integrates information from the environment across different areas. Using neuroimaging, we investigated the spatial pattern of correlated BOLD signal across eight visual areas on data collected during rest conditions and during naturalistic movie viewing. The correlation pattern between areas reflected the underlying receptive field organization with higher correlations between cortical sites containing overlapping representations of visual space. In addition, the correlation pattern reflected the underlying widespread eccentricity organization of visual cortex, in which the highest correlations were observed for cortical sites with iso-eccentricity representations including regions with non-overlapping representations of visual space. This eccentricity-based correlation pattern appears to be part of an intrinsic functional architecture that supports the integration of information across functionally specialized visual areas. DOI: http://dx.doi.org/10.7554/eLife.03952.001

A brief comparative review of primate posterior parietal cortex: A novel hypothesis on the human toolmaker

ABSTRACT The primate visual system contains two major cortical pathways: a ventral‐temporal pathway that has been associated with object processing and recognition, and a dorsal‐parietal pathway that has been associated with spatial processing and action guidance. Our understanding of the role of the dorsal pathway, in particular, has greatly evolved within the framework of the two‐pathway hypothesis since its original conception. Here, we present a comparative review of the primate dorsal pathway in humans and monkeys based on electrophysiological, neuroimaging, neuropsychological, and neuroanatomical studies. We consider similarities and differences across species in terms of the topographic representation of visual space; specificity for eye, reaching, or grasping movements; multi‐modal response properties; and the representation of objects and tools. We also review the relative anatomical location of functionally‐ and topographically‐defined regions of the posterior parietal cortex. An emerging theme from this comparative analysis is that non‐spatial information is represented to a greater degree, and with increased complexity, in the human dorsal visual system. We propose that non‐spatial information in the primate parietal cortex contributes to the perception‐to‐action system aimed at manipulating objects in peripersonal space. In humans, this network has expanded in multiple ways, including the development of a dorsal object vision system mirroring the complexity of the ventral stream, the integration of object information with parietal working memory systems, and the emergence of tool‐specific object representations in the anterior intraparietal sulcus and regions of the inferior parietal lobe. We propose that these evolutionary changes have enabled the emergence of human‐specific behaviors, such as the sophisticated use of tools. HighlightsThe dorsal object system in humans and monkeys supports action guidance.The human dorsal object system mirrors the complexity of the ventral stream.The human dorsal object system is integrated with working memory systems.The human dorsal object system contains unique tool‐specific representations.These may support the human toolmakers sophisticated object‐directed behavior.

Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex

The cerebral cortex is composed of many distinct classes of neurons. Numerous studies have demonstrated corresponding differences in neuronal properties across cell types, but these comparisons have largely been limited to conditions outside of awake, behaving animals. Thus the functional role of the various cell types is not well understood. Here, we investigate differences in the functional properties of two widespread and broad classes of cells in inferior temporal cortex of macaque monkeys: inhibitory interneurons and excitatory projection cells. Cells were classified as putative inhibitory or putative excitatory neurons on the basis of their extracellular waveform characteristics (e.g., spike duration). Consistent with previous intracellular recordings in cortical slices, putative inhibitory neurons had higher spontaneous firing rates and higher stimulus-evoked firing rates than putative excitatory neurons. Additionally, putative excitatory neurons were more susceptible to spike waveform adaptation following very short interspike intervals. Finally, we compared two functional properties of each neurons stimulus-evoked response: stimulus selectivity and response latency. First, putative excitatory neurons showed stronger stimulus selectivity compared with putative inhibitory neurons. Second, putative inhibitory neurons had shorter response latencies compared with putative excitatory neurons. Selectivity differences were maintained and latency differences were enhanced during a visual search task emulating more natural viewing conditions. Our results suggest that short-latency inhibitory responses are likely to sculpt visual processing in excitatory neurons, yielding a sparser visual representation.

Visual short-term memory and motor planning

Despite extensive experimental work showing that memory for visual information in prior fixations is limited, the nature and content of the information maintained across fixations, when vision functions in its natural context, is not well determined. To gain insight into what memory representations might be needed to support vision in the natural world, we examined eye and hand movements while subjects made a sandwich and while they copied a toy model in a virtual environment. Patterns of eye-hand coordination and fixation sequences suggest the need for planning and coordinating movements over a period of a few seconds. Since the movement plan is initiated when the eye is in a different position from that when the movement itself is made, the planning must be in a coordinate frame that is independent of eye position. Movement planning thus requires a representation of the spatial structure in a scene that is built up over different fixations.