Visual, somatosensory, and bimodal activities in the macaque parietal area PEc

Caudal area PE (PEc) of the macaque posterior parietal cortex has been shown to be a crucial node in visuomotor coordination during reaching. The present study was aimed at studying visual and somatosensory organization of this cortical area. Visual stimulations activated 53% of PEc neurons. The overwhelming majority (89%) of these visual cells were best activated by a dark stimulus on a lighter background. Somatosensory stimulations activated 56% of PEc neurons: most were joint neurons (73%); a minority (24%) showed tactile receptive fields, most of them located on the arms. Area PEc has not a clear retinotopy or somatotopy. Among the cells tested for both somatosensory and visual sensitivity, 22% were bimodal, 25% unimodal somatosensory, 34% unimodal visual, and 19% were insensitive to either stimulation. No clear clustering of the different classes of sensory neurons was observed. Visual and somatosensory receptive fields of bimodal cells were not in register. The damage in the human brain of the likely homologous of macaque PEc produces deficits in locomotion and in whole-body interaction with the visual environment. Present data show that macaque PEc has sensory properties and a functional organization in line with the view of an involvement of this area in those processes.     

Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkey

Perception of two- and three-dimensional optic flow critically depends upon extrastriate cortices that are part of the 'dorsal stream' for visual processing. Neurons in area 7a, a sub-region of the posterior parietal cortex, have a dual sensitivity to visual input and to eye position. The sensitivity and selectivity of area 7a neurons to three sensory cues - optic flow, retinotopic stimulus position and eye position - were studied. The visual response to optic flow was modulated by the retinotopic stimulus position and by the eye position in the orbit. The position dependence of the retinal and eye position modulation (i.e. gain field) were quantified by a quadratic regression model that allowed for linear or peaked receptive fields. A local maximum (or minimum) in both the retinotopic fields and the gain fields was observed, suggesting that these sensory qualities are not necessarily linearly represented in area 7a. Neurons were also found that simply encoded the eye position in the absence of optic flow. The spatial tuning for the eye position signals upon stationary stimuli and optic flow was not the same, suggesting multiple anatomical sources of the signals. These neurons can provide a substrate for spatial representation while primates move in the environment.      

Behavioral influences on cortical neuronal responses to optic flow

Optic flow selectively activates neurons in medial superior temporal (MST) cortex. We find that many MST neurons yield larger and more selective responses when the optic flow guides a subsequent eye movement. Smaller, less selective responses are seen when optic flow is preceded by a flashed precue that guides eye movements. Selectivity can decrease by a third (32%) after a flashed precue is presented at a peripheral location as a small spot specifying the target location of the eye movement. Smaller decreases in selectivity (18%) occur when the precue is presented centrally with its shape specifying the target location. Shape precues presented centrally, but not linked to specific target locations, do not appear to alter optic flow selectivity. The effects of spatial precueing can be reversed so that the precue leads to larger and more selective optic flow responses: A flashed precue presented as a distracter before behaviorally relevant optic flow is associated with larger optic flow responses and a 45% increase in selectivity. Together, these findings show that spatial precues can decrease or increase the size and selectivity of optic flow responses depending on the associated behavioral contingencies.     

Inferior parietal lobule projections to anterior inferotemporal cortex (area TE) in macaque monkey

Parietal cortical areas have generally been considered as part of the dorsal stream and, as such, only indirectly connected with inferotemporal cortex. In this report we demonstrate, by using the anterograde tracer BDA, that much of the inferior parietal lobule (IPL) has direct connections to anterior-ventral TE (TEav) around the anterior middle temporal sulcus (amts). Connections from area PG terminate in layers 1 and 5 as well as 4; and those from area PF, target layer 6 of TEav, with a small secondary focus in layer 4 of anterior-dorsal TE. Connections from areas PG and PF are relatively sparse; but those from the mid-IPL region (approximately area PFG), which terminate in layer 4, are light to moderate. In confirmation of these results, injections of retrograde tracers in TEav produce labeled neurons in the IPL. These are most numerous in layer 3 at the border of areas PG and PFG, but also occur in layer 5/6. These laminar patterns are more complex than the classical 'feedforward' or 'feedback' patterns associated with early sensory areas. Branched collaterals are common; and three of seven reconstructed axons branched to both TEav and to the lateral bank of the occipito-temporal sulcus, itself a major source of inputs to TEav. The existence of connections from the IPL preferentially to TEav and the amts provides another example where direct 'bypass' connections operate in parallel with multiple indirect routes. It provides further evidence for the differential connectivity of subdivisions within anterior TE and is consistent with recent evidence from functional magnetic resonance imaging studies that the region around the amts may be part of a network involved in three- dimensional shape, which is distributed across both 'what' and 'where' processing streams.     

Neuronal responses in area 7a to multiple stimulus displays: II. responses are suppressed at the cued location.

Everyday visual scenes contain a variety of stimuli that vary in their significance. The companion paper demonstrates that neurons in the posterior parietal cortex (PPC) are capable of encoding the spatial locations of the salient stimulus in multiple stimulus scenes. The present experiment sought to address how neuronal responses to stimuli appearing in the receptive field are modulated after attention has been drawn to one of multiple stimuli in a visual scene. We recorded from area 7a of the PPC in monkeys trained to do a spatial version of a match-to-sample task. The results show that neuronal responses are greatly suppressed when stimuli appear at previously attended locations. No reduction in responsiveness is observed for locations where stimuli had previously appeared but did not draw attention. These results support the hypothesis that area 7a has a role in redirecting attention to stimuli appearing at novel, unattended locations.     

Cortical neuronal responses to optic flow are shaped by visual strategies for steering

We hypothesized that neuronal responses to virtual self-movement would be enhanced during steering tasks. We recorded the activity of medial superior temporal (MSTd) neurons in monkeys trained to steer a straight-ahead course, using optic flow. We found smaller optic flow responses during active steering than during the passive viewing of the same stimuli. Behavioral analysis showed that the monkeys had learned to steer using local motion cues. Retraining the monkeys to use the global pattern of optic flow reversed the effects of the active-steering task: active steering then evoked larger responses than passive viewing. We then compared the responses of neurons during active steering by local motion and by global patterns: Local motion trials promoted the use of local dot movement near the center of the stimulus by occluding the peripheral visual field midway through the trial. Global pattern trials promoted the use of radial pattern movement by occluding the central visual field midway through the trial. In this study, identical full-field optic-flow stimuli evoked larger responses in global-pattern trials than in local motion trials. We conclude that the selection of specific visual cues reflects strategies for active steering and alters MSTd neuronal responses to optic flow.     

Speed selectivity for optic flow in area 7a of the behaving macaque

Area 7a, in the inferior parietal lobe, has been implicated in optic flow processing to obtain spatial information about the environment. Optic flow, angle-of-gaze and center-of-motion dependencies are already documented, but the selectivity of area 7a to speed is unknown. Such information is crucial as area 7a provides the final step in visual motion analysis that begins at the lateral geniculate nucleus and passes through MT, MST and LIP/VIP. Macaque area 7a neurons were tested with optic flows with speeds of 0.5-128 degrees /s. Of 161 neurons tested in four hemispheres of two adult male macaques, 53% (86/161) were speed selective at either the time of stimulus onset, at the end of the trial, or at both times. Speed selec- tivities resembling the basic filter types (band-pass, band-reject, high-pass, low-pass, broadband) were found. Area 7a neurons exhibited two novel properties not previously reported elsewhere. Speed selectivity was found to be dynamic in that many cells gained, lost or changed speed tuning over the course of a trial. In addition, speed dependence and optic flow selectivity interacted. For example, a cell could preferentially respond to one type of naviga- tional optic flow at a slow speed and a different navigational optic flow at a fast speed. The presence of speed selectivity combined with other properties of area 7a neurons indicates that these neurons may have a role in the concurrent representation of heading as well as multiple object speeds and directions.     

Neuronal responses in area 7a to multiple-stimulus displays: I. neurons encode the location of the salient stimulus.

The primate posterior parietal cortex (PPC) plays an important role in representing and recalling spatial relationships and in the ability to orient visual attention. This is evidenced by the parietal activation observed in brain imaging experiments performed during visuo- spatial tasks, and by the contralateral neglect syndrome that often accompanies parietal lesions. Individual neurons in monkey parietal cortex respond vigorously to the appearance of single, behaviorally relevant stimuli, but little is known about how they respond to more complex visual displays. The current experiments addressed this issue by recording activity from single neurons in area 7a of the PPC in monkeys performing a spatial version of a match-to-sample task. The task required them to locate salient stimuli in multiple-stimulus displays and release a lever after a subsequent stimulus appeared at the same location. Neurons responded preferentially to the appearance of salient stimuli inside their receptive fields. The presence of multiple stimuli did not affect appreciably the spatial tuning of responses in the majority of neurons or the population code for the location of the salient stimulus. Responses to salient stimuli could be distinguished from background stimuli approximately 100 ms after the onset of the cue. These results suggest that area 7a neurons represent the location of the stimulus attracting the animal's attention and can provide the spatial information required for directing attention to a salient stimulus in a complex scene.     

Cerebrovascular responses to subarachnoid blood and serotonin in the monkey.

Preliminary in vitro experiments were performed to determine the serum concentration of serotonin in the monkey, and the ability of cyproheptadine to block serotonin and serum-induced contractions in monkey cerebral arteries. Thirty-four cynomolgus monkeys were subsequently used to study changes in regional cerebral blood flow (CBF) obtained by the intracartoid 133Xe technique, and in the angiographic cerebral arterial caliber resulting from subarachnoid injection of artificial cerebrospinal fluid (CSF), blood, and serotonin. Five animals in each injection group were given 1.0 mg/kg intravenous cyproheptadine (a serotonin-blocking agent) during the post-injection period. Subarachnoid injection of artificial CSF produced no change in CBF or arterial caliber. Post-injection administration of cyproheptadine also had no effect on these parameters. A subarachnoid injection of fresh autogenous blood produced a significant but transient (less than 1 hour) decrease in CBF and moderate vasospasm, which lasted at least 3 hours. This vasospasm was essentially unaffected by intravenous cyproheptadine. The CBF and arterial caliber were unchanged following a subarachnoid injection of serotonin at concentrations (5 x 10(-6)M) present in normal monkey serum. In contrast, 5 x 10(-6) M serotonin invariably produced near maximal contractions in the in vitro cerebral artery preparations. Higher (x10) serotonin concentrations caused a transient CBF response similar to that obtained with blood. However, the cerebral vasospasm induced was of shorter duration than that obtained with blood. These results do not support a major role for serotonin in the production of post-subarachnoid hemorrhage vasospasm. Moreover, our data indicate that in vitro experiments do not reflect the ability of serotonin to constrict cerebral arteries in the intact animal.     

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.     

Neuronal responses in visual area V2 (V2) of macaque monkeys with strabismic amblyopia

Amblyopia, a developmental disorder of spatial vision, is thought to result from a cascade of cortical deficits over several processing stages beginning at the primary visual cortex (V1). However, beyond V1, little is known about how cortical development limits the visual performance of amblyopic primates. We quantitatively analyzed the monocular and binocular responses of V1 and V2 neurons in a group of strabismic monkeys exhibiting varying depths of amblyopia. Unlike in V1, the relative effectiveness of the affected eye to drive V2 neurons was drastically reduced in the amblyopic monkeys. The spatial resolution and the orientation bias of V2, but not V1, neurons were subnormal for the affected eyes. Binocular suppression was robust in both cortical areas, and the magnitude of suppression in individual monkeys was correlated with the depth of their amblyopia. These results suggest that the reduced functional connections beyond V1 and the subnormal spatial filter properties of V2 neurons might have substantially limited the sensitivity of the amblyopic eyes and that interocular suppression was likely to have played a key role in the observed alterations of V2 responses and the emergence of amblyopia.     

Cerebral arterial responses to induced hypertension following subarachnoid hemorrhage in the monkey.

Regional cerebral blood flow (rCBF), angiographic cerebral arterial caliber, and cerebrospinal fluid (CSF) pressure were measured in rhesus monkeys to determine the effect of experimentally induced subarachnoid hemorrhage (SAH) on cerebral arterial responses to graded increases in blood pressure. These measurements were also performed in a control group of monkeys subjected to a mock SAH by injection of artificial CSF into the cerebral space. Before subarachnoid injection of blood or artificial CSF, graded increases in mean arterial blood pressure (MABP) to a level 40% to 50% above baseline values had no effect on rCBF. The major cerebral arteries constricted and CSF pressure remained unchanged. Similar responses were observed after injections of artificial CSF. When MABP was increased in animals that had been subjected to subarachnoid injection of blood, rCBF increased and was associated with dilatation of the major cerebral arteries and moderate increases in CSF pressure. These results demonstrate that cerebral arterial responses to increases in blood pressure may be abnormal in the presence of subarachnoid blood. The manner in which abnormal cerebral arterial reactivity, changes in blood pressure, and vasospasm combine to determine the level of cerebral perfusion following SAH is postulated.     

Spatiotemporal dynamics of the functional architecture for gain fields in inferior parietal lobule of behaving monkey

Intrinsic optical imaging has revealed a representation of eye position smoothly mapped across the surface of the inferior parietal lobule in behaving monkeys. We demonstrate here that blood vessels imaged along with the cortex have large signals tuned sometimes, but not always, to match the surrounding tissue. The relationship between the vessels and surrounding tissue in both space and time was explored using independent component analysis (ICA). Working only with single-trial data, ICA discovered a sequence of regions corresponding to the vascular propagation of activated signals from remote loci into the blood vessels. The vascular signals form a novel map of cortical function--the functional angioarchitecture--superimposed upon the cortical functional architecture. Furthermore, the incorporation of temporal aspects in optical data permitted the tuning of the inferior parietal lobule to be tracked in time through the task, demonstrating the expression of unusual tuning properties that might be exploited for higher cognitive functions.     

Neural activity in primate parietal area 7a related to spatial analysis of visual mazes

Cognitive psychological studies of humans and monkeys solving visual mazes have provided evidence that a covert analysis of the maze takes place during periods of eye fixation interspersed between saccades, or when mazes are solved without eye movements. We investigated the neural basis of this process in posterior parietal cortex by recording the activity of single neurons in area 7a during maze solution. Monkeys were required to determine from a single point of fixation whether a critical path through the maze reached an exit or a blind ending. We found that during this process the activity of approximately one in four neurons in area 7a was spatially tuned to maze path direction. We obtained evidence that path tuning did not reflect a covert saccade plan insofar as the majority of neurons active during maze solution were not active on a delayed-saccade control task, and the minority that were active on both tasks did not exhibit congruent spatial tuning in the two conditions. We also obtained evidence that path tuning during maze solution was not due to the locations of visual receptive fields mapped outside the behavioral context of maze solution, in that receptive field centers and preferred path directions were not spatially aligned. Finally, neurons tuned to path direction were not present in area 7a when a na?ve animal viewed the same visual maze stimuli but did not solve them. These data support the hypothesis that path tuning in parietal cortex is not due to the lower level visual features of the maze stimulus, but rather is associated with maze solution, and as such, reflects a cognitive process applied to a complex visual stimulus.     

Localization of area prostriata and its projection to the cingulate motor cortex in the rhesus monkey

Area prostriata is a poorly understood cortical area located in the anterior portion of the calcarine sulcus. It has attracted interest as a separate visual area and progenitor for the cortex of this modality. In this report we describe a direct projection from area prostriata to the rostral cingulate motor cortex (M3) that forms the fundus and lower bank of the anterior part of the cingulate sulcus. Injections of retrograde tracers in M3 resulted in labeled neurons in layers III, V and VI of prostriate cortex. However, injections of anterograde tracers in M3 did not demonstrate axon terminals in area prostriata. This connection was organized topographically such that the rostral part of M3 received input from the dorsal region of prostriate cortex, whereas middle and caudal levels of M3 received input from more ventral locations. Injections of retrograde and anterograde tracers in the caudal cingulate motor cortex (M4) did not produce labeling in prostriate cortex. Cytoarchitectural analysis confirmed the identity of area prostriata and further clarified its extent and borders with the parasubiculum of the hippocampal formation rostrally, and V1 of the visual cortex caudally. This linkage between cortex bordering V1 and cortex giving rise to a component of the corticofacial and corticospinal pathways demonstrates a more direct visuomotor route than visual association projections coursing laterally.     

Carbon dioxide insufflation attenuates parietal blood flow obstruction in distended colon

BACKGROUND: Bowel distention after colonoscopy has been considered as a cause of blood flow disturbance. Carbon dioxide (CO2), with its higher absorbability and vasodilating effect, may reduce parietal blood flow disturbance of distended colon when used for intraluminal insufflation instead of air. The purpose of this study was to assess parietal blood flow of the colon distended with intraluminal air/CO2 insufflation. METHODS: A 5-cm segment of rat colon was insufflated with either air (air group) or CO2 (CO2 group). Two insufflation methods were employed: temporary insufflation up to an intraluminal pressure of 60 mmHg and continuous insufflation at a pressure of 5, 15, and 30 mmHg. Bowel distention and parietal blood flow measured by laser Doppler imaging were evaluated. RESULTS: For temporary insufflation, bowel distention was prolonged in the air group, whereas it rapidly resolved in the CO2 group. Parietal blood flow decreased in both groups; however, it recovered within 5 min in the CO2 group. For continuous insufflation, under 5 mmHg insufflation, blood flow decreased in the air group, whereas it increased in the CO2 group. Blood flow decreased in both groups under 15 mmHg insufflation; however, it decreased less in the CO2 group. There was a reverse relationship between insufflation pressure and blood flow difference. Inhibition of nitric oxide synthase, ATP-sensitive K+ channel, or heme oxygenase was ineffective against a CO2-induced increase in blood flow. CONCLUSION: CO2 insufflation preserved parietal blood flow not only by rapid resolution of bowel distention but also by its potential vasodilative effect.     

Regional gastric mucosal blood flow after parietal cell vagotomy in dogs

In this study we used the recently validated H2 clearance method to perform endoscopic measurements of gastric mucosal blood flow (MBF) in anesthetized dogs before and after parietal cell vagotomy (PCV). Under resting conditions, MBF in the gastric corpus before PCV was 72 +/- 5 ml/min/100 gm. This was not altered significantly at 4, 8, or 16 weeks after PCV, and there were not significant long-term changes in MBF on the greater or lesser curvatures of the corpus individually. Before PCV infusion of pentagastrin (8 micrograms/kg/hr) elicited increases in corpus MBF to 104 +/- 4 ml/min/100 gm, accompanied by increases in gastric acid output from resting levels of 2.1 +/- 0.9 to 38.6 +/- 2.4 mEq/hr (p less than 0.001). PCV significantly reduced pentagastrin-stimulated acid secretion by 50%, and secretory inhibition was accompanied by significant reductions in pentagastrin-stimulated MBF in the corpus. Pentagastrin did not alter antral MBFs before or after PCV. In summary PCV does not elicit significant long-term changes in resting MBF in different regions of the gastric corpus, and PCV significantly diminishes increases in acid output and corpus MBF that are normally stimulated by pentagastrin. These observations suggest that alterations in gastric MBF after PCV may be attributable to alterations in acid secretion.