A new neural framework for visuospatial processing

Abstract

The division of cortical visual processing into distinct dorsal and ventral streams is a key framework that has guided visual neuroscience. The characterization of the ventral stream as a 'What' pathway is relatively uncontroversial, but the nature of dorsal stream processing is less clear. Originally proposed as mediating spatial perception ('Where'), more recent accounts suggest it primarily serves non-conscious visually guided action ('How'). Here, we identify three pathways emerging from the dorsal stream that consist of projections to the prefrontal and premotor cortices, and a major projection to the medial temporal lobe that courses both directly and indirectly through the posterior cingulate and retrosplenial cortices. These three pathways support both conscious and non-conscious visuospatial processing, including spatial working memory, visually guided action and navigation, respectively.

Figure 1. Frameworks of visuospatial processing

a | The original formulation^,, of the dorsal and ventral streams in the macaque monkey. The ventral stream is a multisynaptic pathway projecting from the striate cortex (area OC) to area TE in the inferior temporal cortex, with a further projection from area TE to ventral prefrontal region FDv. The dorsal stream is a multisynaptic pathway projecting from striate cortex to area PG in the inferior parietal lobule, with a further projection from area PG to dorsolateral prefrontal region FDΔ. On the basis of the effects of lesions in monkeys, the ventral stream was termed a ‘What’ pathway supporting object vision, whereas the dorsal stream was labelled a ‘Where’ pathway supporting spatial vision. b | The top panel depicts the location of the lesions in patient D.F. (shown in blue and indicated by white arrows) that led to impairment in object perception but not in the accuracy of orienting her hand when reaching to the same objects. This pattern of results led to the proposal^,, depicted in the bottom panel, that the dorsal stream is more accurately characterized as a motoric ‘How’ pathway supporting visually guided action than as a perceptual ‘Where’ pathway. c | The new neural framework for dorsal stream function that is proposed in this Review. At least three distinct pathways emanate from the posterior parietal cortex. One pathway targets the prefrontal cortex (shown by a dashed green arrow; see also part a) and supports spatial working memory (the parieto–prefrontal pathway); a second pathway targets the premotor cortex (shown by a dashed red arrow) and supports visually-guided actions (the parieto–premotor pathway); and the third targets the medial temporal lobe, both directly and through the posterior cingulate and retrosplenial areas (shown by a dashed blue arrow), and supports navigation (the parieto–medial temporal pathway). PCC, posterior cingulate cortex; RSC, retrosplenial cortex; TE, rostral inferior temporal cortex; TEO, posterior inferior temporal cortex; V1, visual area 1 (also known as primary visual cortex). Part b, top panel is modified, with permission, from REF. © (2003) Oxford Journals.

Figure 2. Anatomy of the three pathways

a | The complexity of the occipito–parietal connections (shown by black arrows) on standard medial and lateral views of a rhesus monkey brain. The parts of visual area 1 (V1; also known as the primary visual cortex) that represent the central as well as peripheral visual fields are strongly connected with middle temporal area (MT) through visual areas V2, V3 and V4. By contrast, the parts of V1 that represent both the central and peripheral visual fields project through visual areas V2, V3 and V3A to a retinotopically organized and functionally distinct area V6 on the rostral bank of the parieto-occipital sulcus (pos). The visual information from area V6 reaches the parietal lobe through two main channels: one projecting medially to the bimodal (visual and somatosensory) area V6A and medial intraparietal area (MIP), which are located on the rostral bank of pos and the medial bank of the caudal intraparietal sulcus (ips), respectively; and the other projecting laterally to lateral intraparietal area (LIP) and ventral intraparietal area (VIP) in the ips and to areas MT and MST in the caudal superior temporal sulcus (sts). All of these posterior parietal areas are strongly connected with each other and with the surface cortex of the inferior parietal lobule (IPL). Feed-forward projections from lower- to higher-level processing areas (shown by single-ended arrows in the main figure) are usually reciprocated by feedback projections (not shown) from higher to lower areas; connections between areas at the same hierarchical level are shown by double-ended arrows in the main figure. The inset, which illustrates the findings from a study by Rozzi et al., depicts connections of IPL subdivisions with the posterior cingulate cortex (PCC) and ventral premotor area F5. Note that areas Opt and PG (subdivisions of the caudal IPL (cIPL)), which are primarily visual, appear to have stronger reciprocal connections with the PCC than with F5 (thick versus thin lines). The reverse holds for areas PFG and PF (subdivisions of the rostral IPL (rIPL)), which are primarily somatosensory. b | The sources and targets of the three pathways that emerge from the parietal component of the occipito–parietal circuit (also known as the dorsal stream). The parieto–prefrontal pathway (shown by green arrows) links areas LIP, VIP and MT/MST with a pre-arcuate region (area 8A; the frontal eye-field) and the caudal part of the principal sulcus in the lateral prefrontal cortex (area 46) — targets that serve eye movement control and spatial working memory, respectively. The parieto–premotor pathway (shown by red arrows) links areas V6A and MIP with the dorsal premotor cortex (areas F2 and F7), and also links area VIP with the ventral premotor cortex (areas F4 and F5) — targets that serve visually guided eye movements, reaching and grasping. The parieto–medial temporal pathway (shown by blue arrows; thick, thin and dashed lines represent dense, moderate and light projections, respectively) originates in the cIPL — that is, areas Opt and PG (see part a, inset) — and projects to subdivisions of the hippocampus (CA1/prosubiculum (proS), and presubiculum (preS)/parasubiculum (paraS)), both directly and indirectly via the PCC (areas 31 and 23), retrosplenial cortex (RSC; areas 29 and 30) and the posterior parahippocampal cortex (areas TF and TH in the rostral portion, and area TFO in the caudal portion) — targets that enable navigation and route learning. 23v, ventral subregion of the posterior cingulate; 28, entorhinal cortex; 35 and 36, perirhinal cortex; as, arcuate sulcus; cas, calcarine sulcus; CC, corpus callosum; cis, cingulate sulcus; cs, central sulcus; ios, inferior occipital sulcus; ls, lateral sulcus; ots, occipitotemporal sulcus; PGm, medial parietal area (also known as 7m); ps, principal sulcus; TE, rostral inferior temporal cortex; TEav, anterior ventral subregion of TE; TEOv, ventral subregion of TEO; TEpv, posterior ventral subregion of TE.

Figure 3. Parieto–medial temporal pathway in humans

This figure is based on resting-state MRI functional connectivity of the precuneus in humans. Medial parietal area PGm (also known as 7m) and area V6 (part of parieto-occipital area PO) in the caudal part of the medial surface show strong functional connectivity (black lines) with the angular gyrus, the likely human homologue of the caudal inferior parietal lobule (cIPL). V6 also shows strong connectivity with early visual areas in the region of the calcarine sulcus (cs), reflecting a network that is the presumptive human homologue of the occipito–parietal network observed in monkeys (FIG. 2a). Similarly, the posterior cingulate cortex (PCC, areas 23 and 31) and the retrosplenial cortex (RSC, areas 29 and 30), on the medial surface, show strong functional connectivity (shown by blue lines) with both cIPL and the parahippocampal gyrus in the medial temporal lobe, reflecting a network that is the presumptive human homologue of the parieto–medial temporal pathway observed in monkeys (FIG. 2b). ips, intraparietal sulcus; pos, parieto–occipital sulcus; SPL, superior parietal lobule. Figure is modified, with permission, from REF. © (2009) National Academy of Sciences.

Figure 4. Functional evidence from PCC and RSC

a | Design and results of a study by Dean and Platt. Monkeys fixated the centre of the screen, after which a target appeared in one of ten positions across the upper visual field (top panel). After a delay, the central fixation cross disappeared and monkeys made an eye movement to the target. To determine whether a neuron encoded the position of the target in allocentric (that is, world- or screen-centred coordinates) or egocentric coordinates, monkeys’ heads were rotated, thus changing the egocentric but not allocentric position of the target (middle panel). Neurons in the posterior cingulate cortex (PCC) encoded target location in both allocentric and egocentric coordinates with a bias towards allocentric coding (bottom panel). b | Design and results of a study by Hashimoto, Tanaka and Nakano. Three patients with lesions of the retrosplenial cortex (RSC) were tested for their ability to coordinate allocentric and egocentric representations. Patients were placed in the middle of a 3 × 3 grid with three objects arrayed around them. After a study period, the patients closed their eyes, the objects were removed and the patients then had to recreate the array (middle panel). When patients were rotated before recreating the array, their performance was significantly impaired compared with the control situation (bottom panel), suggesting a deficit in coordinating egocentric and allocentric representations after changes in egocentric position. Part a is reproduced, with permission, from REF. © (2006) Society for Neuroscience. Part b, data in the bottom panel are from REF. .

Figure 5. Functional evidence from retrosplenial complex and medial temporal lobe

a | Location of the retrosplenial complex averaged across 38 participants. Notably, the location of this area is similar to that of the lesions described in FIG. 4b. b | Functional MRI response magnitude of the retrosplenial complex to different aspects of visual scenes. Retrosplenial complex responses were high when participants were asked to judge whether the depicted familiar scene was located to the east or west of a reference point (‘location’) and, separately, whether the image was taken facing to the east or west (‘orientation’). Retrosplenial complex responses were comparatively lower when participants made familiarity judgments about scenes, with the greatest reduction occurring in response to unfamiliar, as compared to familiar, scenes. c | Location of the parahippocampal place area (PPA) in the medial temporal lobe (MTL) averaged across 38 participants. d | fMRI response magnitude of the PPA to five different visual stimuli. PPA responses were far higher for scenes than for either single or multiple objects, and were equally high for both furnished and empty rooms. Parts a and c are reproduced, with permission, from REF. © (2008) Cell Press. Part b is modified, with permission, from REF. © (2007) Society for Neuroscience. Part d is modified, with permission, from REF. © Macmillan Publishers Ltd. All rights reserved.