Direct Temporal-Occipital Feedback Connections to Striate Cortex (V1) in the Macaque Monkey

Although there have been reports of sparse projections fromtemporal areas TE, TF, and even TH to area V1, it is generallybelieved that cortical afferents to V1 originate exclusivelyfrom prestriate areas. Injections of anterograde tracers inanterior occipital and temporal areas, however, consistentlyproduce labeled terminals in area V1. In order to confirm theseresults and display the full range of foci projecting to V1,we injected V1 in two monkeys with the retrograde tracer fastblue. Feedback connections were found, as expected, from severalprestriate areas (V2, V3, V4, and MT). These originate fromneurons in layers 3A and 6. Connections were also found fromseveral more distal regions, namely, areas TEO, TE, TF, TH,and from cortex in the occipitotemporal and superior temporal(STS) sulci. Filled neurons occurred in two small foci in thecaudal intraparietal sulcus. These more distal feedback connectionstend to originate only from layer 6. An additional injectionof the retrograde tracer diamidino yellow in area V2 of oneanimal revealed a similarly widespread network of feedback connections.In some areas (In the STS and in TEO), 10–15% of fluorescentneurons were double-labeled. These results indicate that feedback connections to early visualcortex derive from a widespread network of areas, includinglimbic-associated cortices. These connectional patterns testifyto the massive recursiveness of anatomical pathways. As thereare no reports of projections from V1 to anterior temporal cortices,our results also indicate that some cortical feedback connectionsmay not be strictly reciprocal.     

Cortical projections of area V2 in the macaque

To determine the locus, extent and topograhic organization of cortical projections of area V2, we injected tritiated amino acids under electrophysiological control into 15 V2 sites in 14 macaques. The injection sites included the foveal representation and representations ranging from central to far peripheral eccentricities in both the upper and lower visual fields. The results indicated that all V2 sites project topographically back to V1 and forward to V3, V4 and MT. There is also a topographically organized projection from V2 to V4t, but this projection is limited to the lower visual field representation. V2 thus appears to project to virtually all the visual cortex within the occipital lobe. In addition to these projections to occipital visual areas, V2 sites representing eccentricities of approximately 30 degrees and greater project to three visual areas in parietal cortex-the medial superior temporal (MST), parieto-occipital (PO) and ventral intraparietal (VIP) areas. This peripheral field representation of V2 also projects to area VTF, a visual area located in area TF on the posterior parahippocampal gyrus. Projections from the peripheral field representation of V2 of parietal areas could provide a direct route for rapid activation of circuits serving spatial vision and spatial attention.      

Connections of Inferior Temporal Areas TEO and TE with Parietal and Frontal Cortex in Macaque Monkeys

Inferior temporal cortex is perhaps the highest visual processingarea and much anatomical work has focused on its connectionswith other visual areas in temporal and occipital cortex. Herewe report connections of inferior temporal cortex with regionsin the frontal and parietal lobes. Inferior temporal areas TEOand TE were injected with WGA-HRP and ³H-AA, respectively, orvice versa, in 1-week-old infant and 3–4–year-oldadult monkeys (Macaca mulatta). The results indicated that whereasTEO has more extensive connections with parietal areas, TE hasmore extensive connections with prefrontal areas. Thus, in theintraparietal sulcus, area TEO is connected with areas LIPd,LIPv, and V3A, and with the as yet undefined region betweenLIPv and V3A, whereas the connections of TE are predominantlywith LIPd, and to a lesser extent with LIPv. In the prefrontalcortex, area TE is connected with areas 8 and 45 in the inferiorlimb of the anterior bank of the arcuate sulcus, with area 12on the inferior prefrontal convexity, and with areas 11 and13 on the orbital surface. By contrast, the connections of areaTEO are limited to areas 8, 45, and 12. Furthermore, withinprefrontal cortex, the projections from areas TEO and TE terminatein different layers in areas 8 and 45, such that those fromTEO terminate in all layers, whereas those from TE terminatein layers I and V/VI only. In contrast to the connections ofareas TEO and TE with various medical temporal-lobe and subcorticalstructures, which are immature in infant monkeys (Webster etal., 1991, 1993b), the connections with parietal and prefrontalareas appear adult-like as early as 1 week of age.     

On the emergence of primary visual perception

We propose a concise novel conceptual and biological framework for the analysis of primary visual perception (PVP) that refers to the most basic levels of our awake subjective visual experiences. Neural representations for image content elaborated within V1/V2 and the early occipitotemporal (ventral) loop remain only latent with respect to PVP until spatially localized with respect to an attending observer. This process requires more than the downstream deployment of attentional resources onto targeted neurons. Additionally, the source neurons for such processes must be linked to a neural representation subserving a first-person perspective. We hypothesize that the simultaneous emergence of both the perceptual experience of image content and the personal inference of its ownership requires the resolution of any conflicting neuronal signaling between afferent and recurrent projections within and between both the ventral and dorsal streams. The V1/V2 complex and ventral cortical areas V3 and the V4 complex together with dorsal cortical areas LIP, VIP, and 7a with additional contributions from the motion areas V5/MT (middle temporal area), FST (fundus of superior temporal area), and MST (medial superior temporal area) together with their subcortical dependencies have the physiological properties required to constitute a "posterior perceptual core" that encodes the normal primary perceptual experience of image content, space, and sense of minimal self.     

Impaired filtering of distracter stimuli by TE neurons following V4 and TEO lesions in macaques

Directing attention to a behaviorally relevant visual stimulus can overcome the distracting effects of other nearby stimuli. Correspondingly, physiological studies indicate that attention serves to filter distracting stimuli from receptive fields (RFs) in several extrastriate areas. Moreover, a recent study demonstrated that lesions of extrastriate areas V4 and TEO produce impairments in attentional filtering. A critical remaining question concerns why lesions of ventral stream areas cause attentional filtering impairments. To address this question, we tested the effects of restricted area V4 and TEO lesions on both behavioral performance and the responses of downstream neurons in area TE. The lesions impaired behavioral discrimination thresholds and altered neuronal selectivity for target stimuli in the presence of distracters. With attention to the target, but in the absence of V4 and/or TEO inputs, TE neurons responded as though attentional inputs could no longer be used to filter distracters from their RFs. This presumably occurred because top-down attentional signals were no longer able to filter distracters from the RFs of the cells that provide TE with major input. Consistent with this interpretation, increasing the spatial separation between targets and distracters, such that they no longer fell within a typical V4 RF dimension, restored both behavioral performance and neuronal selectivity in the portion of TE RFs affected by the V4 lesion.     

Organization of horizontal axons in the inferior temporal cortex and primary visual cortex of the macaque monkey

We investigated the organization of horizontal connections at two distinct hierarchical levels in the ventral visual cortical pathway of the monkey, the inferior temporal (TE) and primary visual (V1) cortices. After injections of anterograde tracers into layers 2 and 3, clusters of terminals ('patches') of labeled horizontal collaterals in TE appeared at various distances up to 8 mm from the injection site, while in V1 clear patches were distributed only within 2 mm. The size and spacing of these patches in TE were larger and more irregular than those observed in V1. The labeling intensity of patches in V1 declined sharply with distance from the injection site. This tendency was less obvious in TE; a number of densely labeled patches existed at distant sites beyond weakly labeled patches. While injections into both areas resulted in an elongated pattern of patches, the anisotropy was greater in TE than in V1 for injections of a similar size. Dual tracer injections and larger-sized injections further revealed that the adjacent sites in TE had spatially distinct horizontal projections, compared to those in V1. These area-specific characteristics of the horizontal connections may contribute to the differences in visual information processing of TE and V1.     

Quantitative analysis of the corticocortical projections to the middle temporal area in the marmoset monkey: evolutionary and functional implications

The connections of the middle temporal area (MT) were investigated in the marmoset, one of the smallest primates. Reflecting the predictions of studies that modeled cortical allometric growth and development, we found that in adult marmosets MT is connected to a more extensive network of cortical areas than in larger primates, including consistent connections with retrosplenial, cingulate, and parahippocampal areas and more widespread connections with temporal, frontal, and parietal areas. Quantitative analyses reveal that MT receives the majority of its afferents from other motion-sensitive areas in the temporal lobe and from the occipitoparietal transition areas, each of these regions containing approximately 30% of the projecting cells. Projections from the primary visual area (V1) and the second visual area (V2) account for approximately 20% of projecting neurons, whereas "ventral stream" and higher-order association areas form quantitatively minor projections. A relationship exists between the percentage of supragranular layer neurons forming the projections from different areas and their putative hierarchical rank. However, this relationship is clearer for projections from ventral stream areas than it is for projections from dorsal stream or frontal areas. These results provide the first quantitative data on the connections of MT and extend current understanding of the relationship between cortical anatomy and function in evolution.     

Cortical connections of the macaque anterior intraparietal (AIP) area

We traced the cortical connections of the anterior intraparietal (AIP) area, which is known to play a crucial role in visuomotor transformations for grasping. AIP displayed major connections with 1) areas of the inferior parietal lobule convexity, the rostral part of the lateral intraparietal area and the SII region; 2) ventral visual stream areas of the lower bank of the superior temporal sulcus and the middle temporal gyrus; and 3) the premotor area F5 and prefrontal areas 46 and 12. Additional connections were observed with the caudal intraparietal area and the ventral part of the frontal eye field. This study suggests that visuomotor transformations for object-oriented actions, processed in AIP, rely not only on dorsal visual stream information related to the object's physical properties but also on ventral visual stream information related to object identity. The identification of direct anatomical connections with the inferotemporal cortex suggests that AIP also has a unique role in linking the parietofrontal network of areas involved in sensorimotor transformations for grasping with areas involved in object recognition. Thus, AIP could represent a crucial node in a cortical circuit in which hand-related sensory and motor signals gain access to representations of object identity for tactile object recognition.     

Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex

We compared the morphological characteristics of layer III pyramidal neurones in different visual areas of the occipitotemporal cortical 'stream', which processes information related to object recognition in the visual field (including shape, colour and texture). Pyramidal cells were intracellularly injected with Lucifer Yellow in cortical slices cut tangential to the cortical layers, allowing quantitative comparisons of dendritic field morphology, spine density and cell body size between the blobs and interblobs of the primary visual area (V1), the interstripe compartments of the second visual area (V2), the fourth visual area (V4) and cytoarchitectonic area TEO. We found that the tangential dimension of basal dendritic fields of layer III pyramidal neurones increases from caudal to rostral visual areas in the occipitotemporal pathway, such that TEO cells have, on average, dendritic fields spanning an area 5-6 times larger than V1 cells. In addition, the data indicate that V1 cells located within blobs have significantly larger dendritic fields than those of interblob cells. Sholl analysis of dendritic fields demonstrated that pyramidal cells in V4 and TEO are more complex (i.e. exhibit a larger number of branches at comparable distances from the cell body) than cells in V1 or V2. Moreover, this analysis demonstrated that the dendrites of many cells in V1 cluster along specific axes, while this tendency is less marked in extrastriate areas. Most notably, there is a relatively large proportion of neurones with 'morphologically orientation-biased' dendritic fields (i.e. branches tend to cluster along two diametrically opposed directions from the cell body) in the interblobs in V1, as compared with the blobs in V1 and extrastriate areas. Finally, counts of dendritic spines along the length of basal dendrites revealed similar peak spine densities in the blobs and the interblobs of V1 and in the V2 interstripes, but markedly higher spine densities in V4 and TEO. Estimates of the number of dendritic spines on the basal dendritic fields of layer III pyramidal cells indicate that cells in V2 have on average twice as many spines as V1 cells, that V4 cells have 3.8 times as many spines as V1 cells, and that TEO cells have 7.5 times as many spines as V1 cells. These findings suggest the possibility that the complex response properties of neurones in rostral stations in the occipitotemporal pathway may, in part, be attributed to their larger and more complex basal dendritic fields, and to the increase in both number and density of spines on their basal dendrites.      

Cortical connections of the inferior parietal cortical convexity of the macaque monkey

We traced the cortical connections of the 4 cytoarchitectonic fields--Opt, PG, PFG, PF--forming the cortical convexity of the macaque inferior parietal lobule (IPL). Each of these fields displayed markedly distinct sets of connections. Although Opt and PG are both targets of dorsal visual stream and temporal visual areas, PG is also target of somatosensory and auditory areas. Primary parietal and frontal connections of Opt include area PGm and eye-related areas. In contrast, major parietal and frontal connections of PG include IPL, caudal superior parietal lobule (SPL), and agranular frontal arm-related areas. PFG is target of somatosensory areas and also of the medial superior temporal area (MST) and temporal visual areas and is connected with IPL, rostral SPL, and ventral premotor arm- and face-related areas. Finally, PF is primarily connected with somatosensory areas and with parietal and frontal face- and arm-related areas. The present data challenge the bipartite subdivision of the IPL convexity into a caudal and a rostral area (7a and 7b, respectively) and provide a new anatomical frame of reference of the macaque IPL convexity that advances our present knowledge on the functional organization of this cortical sector, giving new insight into its possible role in space perception and motor control.     

Connection patterns distinguish 3 regions of human parietal cortex

Three regions of the macaque inferior parietal lobule and adjacent lateral intraparietal sulcus (IPS) are distinguished by the relative strengths of their connections with the superior colliculus, parahippocampal gyrus, and ventral premotor cortex. It was hypothesized that connectivity information could therefore be used to identify similar areas in the human parietal cortex using diffusion-weighted imaging and probabilistic tractography. Unusually, the subcortical routes of the 3 projections have been reported in the macaque, so it was possible to compare not only the terminations of connections but also their course. The medial IPS had the highest probability of connection with the superior colliculus. The projection pathway resembled that connecting parietal cortex and superior colliculus in the macaque. The posterior angular gyrus and the adjacent superior occipital gyrus had a high probability of connection with the parahippocampal gyrus. The projection pathway resembled the macaque inferior longitudinal fascicle, which connects these areas. The ventral premotor cortex had a high probability of connection with the supramarginal gyrus and anterior IPS. The connection was mediated by the third branch of the superior longitudinal fascicle, which interconnects similar regions in the macaque. Human parietal areas have anatomical connections resembling those of functionally related macaque parietal areas.     

Search for color 'center(s)' in macaque visual cortex

It is often stated that color is selectively processed in cortical area V4, in both macaques and humans. However most recent data suggests that color is instead processed in region(s) antero-ventral to V4. Here we tested these two hypotheses in macaque visual cortex, where 'V4' was originally defined, and first described as color selective. Activity produced by equiluminant color-varying (versus luminance-varying) gratings was measured using double-label deoxyglucose in awake fixating macaques, in multiple areas of flattened visual cortex. Much of cortex was activated near-equally by both color- and luminance-varying stimuli. In remaining cortical regions, discrete color-biased columns were found in many cortical visual areas, whereas luminance-biased activity was found in only a few specific regions (V1 layer 4B and area MT). Consistent with a recent hypothesis, V4 was not uniquely specialized for color processing, but areas located antero-ventral to V4 (in/near TEO and anterior TE) showed more color-biased activity.     

The parahippocampal gyrus in the baboon: anatomical, cytoarchitectonic and magnetic resonance imaging (MRI) studies

The parahippocampal gyrus, located at the medial temporal lobe, is a key structure in declarative memory processing. We have analyzed the general organization of the parahippocampal gyrus in the baboon, a nonhuman primate species relatively close to human. This region is rostrocaudally made up of the temporopolar, perirhinal, entorhinal (divided into seven subfields) and posterior parahippocampal (areas TH and TF) cortices. The basic analysis has been performed in three brains, serially sectioned and stained with thionin, myelin stain, acetylcholinesterase and parvalbumin, to determine cytoarchitectonic boundaries. Borders of all subfields were charted onto camera lucida drawings, and two-dimensional maps of the surface and topography of the parahippocampal gyrus were made. Finally, the limits of each parahippocampal area were then transposed on corresponding MR images (commonly used for in vivo PET or functional MRI activation studies) of two animals for precise identification. The general cytoarchitectonic features of the baboon parahippocampal gyrus are similar to macaques, but the size of temporopolar cortex and the laminar organization of perirhinal and posterior parahippocampal cortices resemble humans more than macaque species. In conclusion, the size and structure of the baboon parahippocampal cortex makes this species very appropriate for experimental studies on memory function.     

Comparison of Dendritic Fields of Layer III Pyramidal Neurons in Striate and Extrastriate Visual Areas of the Marmoset: a Lucifer Yellow Intracellular Injection Study

Basal dendritic field areas of layer III pyramidal neurons werecompared between the first (V1), second (V2), dorsolateral (DL)and fundus of the superior temporal (FST) areas in marmosetmonkey visual cortex. These areas correspond to early stagesof visual processing (V1, V2) and to areas specialized for theanalysis of shape (DL) and motion (FST). Neurons in fixed tangentialcortical slices (250 µm) were injected with Lucifer Yellowand immunohistochemically processed for a diaminobenzidine reactionproduct Dendritic field areas were calculated for layer IIIpyramidal cells whose complete basal projection was judged tobe within the section (n = 189). Borders between different visualareas were established based on cytochrome oxidase immunohistochemistryand myelin patterns in the experimental hemisphere, and electrophysiologicalrecordings in the contralateral hemisphere. Pyramidal neuronsin V1 had a mean basal dendritic field area of 1.84 x 10⁴ µm²(SEM = 2.04 = 2.04 x 10³ µm²;n = 21). Layer III pyramidalcells in V2 had a mean basal dendritic field 1.26 times larger(mean = 2.32 x 10⁴ ± 1.78 x 10³ n = 42) than that ofV1 neurons. The mean dendritic field area of layer III pyramidalcells in DL (n = 76) was 1.5 times larger than that in V1 (mean= 2.75 x 10⁴ ± 1.59 x 10³ µm²) and that in FST(n = 50) was 2.3 times larger (mean = 4.26 x 10⁴ ± 2.79x 10³ µm²). Our results show that there is a correlationbetween tangential dendritic field area of basal dendrites oflayer III pyramidal neurons and modality of visual processing.The increase in basal dendritic field area of layer III pyramidalcells may allow more extensive sampling of inputs as requiredby higher-order processing of visual information.     

Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain

Visual changes in feature movies, like in real-live, can be partitioned into global flow due to self/camera motion, local/differential flow due to object motion, and residuals, for example, due to illumination changes. We correlated these measures with brain responses of human volunteers viewing movies in an fMRI scanner. Early visual areas responded only to residual changes, thus lacking responses to equally large motion-induced changes, consistent with predictive coding. Motion activated V5+ (MT+), V3A, medial posterior parietal cortex (mPPC) and, weakly, lateral occipital cortex (LOC). V5+ responded to local/differential motion and depended on visual contrast, whereas mPPC responded to global flow spanning the whole visual field and was contrast independent. mPPC thus codes for flow compatible with unbiased heading estimation in natural scenes and for the comparison of visual flow with nonretinal, multimodal motion cues in it or downstream. mPPC was functionally connected to anterior portions of V5+, whereas laterally neighboring putative homologue of lateral intraparietal area (LIP) connected with frontal eye fields. Our results demonstrate a progression of selectivity from local and contrast-dependent motion processing in V5+ toward global and contrast-independent motion processing in mPPC. The function, connectivity, and anatomical neighborhood of mPPC imply several parallels to monkey ventral intraparietal area (VIP).     

Cortical input to the frontal pole of the marmoset monkey

We used fluorescent tracers to map the pattern of cortical afferents to frontal area 10 in marmosets. Dense projections originated in several subdivisions of orbitofrontal cortex, in the medial frontal cortex (particularly areas 14 and 32), and in the dorsolateral frontal cortex (particularly areas 8Ad and 9). Major projections also stemmed, in variable proportions depending on location of the injection site, from both the inferior and superior temporal sensory association areas, suggesting a degree of audiovisual convergence. Other temporal projections included the superior temporal polysensory cortex, temporal pole, and parabelt auditory cortex. Medial area 10 received additional projections from retrosplenial, rostral calcarine, and parahippocampal areas, while lateral area 10 received small projections from the ventral somatosensory and premotor areas. There were no afferents from posterior parietal or occipital areas. Most frontal connections were balanced in terms of laminar origin, giving few indications of an anatomical hierarchy. The pattern of frontopolar afferents suggests an interface between high-order representations of the sensory world and internally generated states, including working memory, which may subserve ongoing evaluation of the consequences of decisions as well as other cognitive functions. The results also suggest the existence of functional differences between subregions of area 10.     

Some temporal and parietal cortical connections converge in CA1 of the primate hippocampus.

Large sectors of polymodal cortex project to the hippocampal formation via convergent input to the entorhinal cortex. The present study reports an additional access route, whereby several cortical areas project directly to CA1. These are parietal areas 7a and 7b, area TF medial to the occipitotemporal sulcus (OTS), and a restricted area in the lateral bank of the OTS that may be part of ventromedial area TE. These particular cortical areas are implicated in visuospatial processes; and their projection to and convergence within CA1 may be significant for the elaboration of 'view fields', for the postulated role of the hippocampal formation in topographic learning and memory, or for the snapshot identification of objects in the setting of complex visuospatial relationships. Convergence of vestibular and visual inputs (from areas 7b and 7a respectively) would support previous physiological findings that hippocampal neurons respond to combinations of whole-body motion and a view of the environment. The direct corticohippocampal connections are widely divergent, especially those from the temporal areas, which extend over much of the anteroposterior axis of the hippocampal main body. Divergent connections potentially influence large populations of CA1 pyramidal neurons, consistent with the suggestion that these neurons are involved in conjunctive coding. The same region of ventromedial TE, besides the direct connections to CA1, also gives rise to direct projections to area V1, and may correspond to a functionally specialized subdivision, perhaps part of VTF.     

Modulation of LIP activity by predictive auditory and visual cues

The lateral intraparietal area (area LIP) contains a multimodal representation of extra-personal space. To further examine this representation, we trained rhesus monkeys on the predictive-cueing task. During this task, monkeys shifted their gaze to a visual target whose location was predicted by the location of an auditory or visual cue. We found that, when the sensory cue was at the same location as the visual target, the monkeys' mean saccadic latency was faster than when the sensory cue and the visual target were at different locations. This difference in mean saccadic latency was the same for both auditory cues and visual cues. Despite the fact that the monkeys used auditory and visual cues in a similar fashion, LIP neurons responded more to visual cues than to auditory cues. This modality-dependent activity was also seen during auditory and visual memory-guided saccades but to a significantly greater extent than during the predictive-cueing task. Additionally, we found that the firing rate of LIP neurons was inversely correlated with saccadic latency. This study indicates further that modality-dependent differences in LIP activity do not simply reflect differences in sensory processing but also reflect the cognitive and behavioral requirements of a task.     

Evidence for Visual Cortical Area Homologs in Cat and Macaque Monkey

The maps of visuotopically discrete visual cerebral corticalareas in the cat and the macaque monkey are compared and gapsin knowledge are identified that limit such comparisons. Catareas 17, 18, and 19 can be equated with macaque areas VI, V2,and V3, respectively, based on criteria of relative positionin the cortical mantle, internal organization of visual fieldrepresentations, and trans- and subcortical connections. Usingthese same criteria, a visual area on the medial bank of thelateral suprasylvian sulcus (area PMLS) in the cat can be equatedwith macaque area V5. The equivalences are supported by dataon neuronal receptive field properties and the contributionsthe areas make to visual behavior. Although the data are scantyfor most other visual areas, there are enough data tentativelyto equate collectively cat areas 20a and 20b with macaque areasTF and TH and to liken cat areas 21a and 21b with macaque areaV4. What is not clear is if there is a region in cat that isequivalent to area TE in the macaque monkey. If there is, itlikely lies on the banks of the posterior suprasylvian sulcusbetween areas 20 and 21 and the polysensory cortex of the posteriorectosylvian gyrus. Knowledge gained from prior research on macaqueareas V4 and TE can be used to formulate specific additionalinvestigations of cat area 21 and the uncharted posterior suprasylviansulcus. In addition, prior investigations carried out on catarea 20 can be used to devise specific explorations of macaqueareas TF and TH.