Neuronal responses in macaque area PEc to saccades and eye position.

Neurons in area PEc in the superior parietal cortex encode signals from different modalities, such as visual, extraretinal and somatosensory, probably combining them to encode spatial parameter of extrapersonal space to prepare body movements. This study reports the characterization of the functional properties of PEc non-visual neurons that showed saccade-related activity. We analyzed the pre- and post-saccadic firing activity in 189 neurons recorded in five hemispheres of three behaving monkeys. Spiking activity of PEc single neurons was recorded while the monkeys performed visually-guided saccades in a reaction time task. We found that 84% of neurons recorded from area PEc showed pre-saccadic activity with directional tuning. In 26% of neurons, we found inhibition of activity in the pre-saccadic period. The onset of this "pause" always started before the saccade and, in 51% of neurons, it was invariant among different gaze directions. The post-saccadic activity in these cells was either a phasic response with directional tuning (77%) and/or an eye position tuning (75%). The analysis of the preferred direction did not show hemispheric preference, however, for the majority of neurons, the angular difference in the preferred direction, in the pre- and post-saccadic period, was more than 60 degrees . By confirming, therefore, that PEc neurons carry information about eye position, these novel findings open new horizons on PEc function that, to date, is not well documented. The pre-saccadic activity may reflect an involvement in saccade control, whereas post-saccadic activity may indicate a role in informing on the new eye position. These novel results about saccade and eye position processing may imply a role of area PEc in gaze direction mechanisms and, possibly, in remapping visual space after eye movements.

Visual motion responses of neurons in the caudal area pe of macaque monkeys.

Area PE of macaques has traditionally been considered a somatosensory association cortex. Recent studies, however, suggest that neurons of this and neighboring areas are involved in the visual control of movement, especially arm movement. We investigated the neuronal sensitivity to local visual stimuli of this region by recording neuronal activity in two behaving macaque monkeys trained in a simple visual fixation task. Recordings were performed from the dorsal surface of the caudal pole of the superior parietal lobule (SPL). Classical receptive fields (RFs) were mapped by using conventional static or moving luminous figures. We found that many neurons in this area were selectively activated by moving visual stimuli. Cell responses were tuned to the movement direction. RFs were usually large; their mean surface covered some 30 x 30 degrees of the visual field. The fovea was often included into RF, in many cases it was along a RF side. The center of RFs was mainly located in the contralateral hemifield, although RFs having the center ipsilaterally sited were also found. No evident retinotopy was found. Visual neurons were especially concentrated in a region of the SPL likely corresponding to area PEc. These results suggest that the caudal part of area PE contains neuronal populations specifically signaling local visual motion, possibly encoding the direction of moving objects. These signals might well be suited for sensorimotor integration mechanisms aimed at motor acts.

Projections from visual cortical areas of the superior temporal sulcus to the lateral terminal nucleus of the accessory optic system in macaque monkeys.

Tritiated amino acids were injected into the striate area and in single visual areas of the superior temporal sulcus (STS) of 7 cynomolgus monkeys, in order to trace visual cortical projections to the nuclei of the accessory optic system (AOS). Injections in STS separately involved the areas MT and MST, and resulted in labels within the lateral terminal nucleus of the AOS. In no case were labels found within the AOS nuclei in the brains injected in the striate area, or within the contralateral AOS. It seems likely that the areas MT and MST contribute signals--selectively related to visual motion processing--to the AOS, which is probably involved in the neuronal pathway subserving the optokinetic reflex.

Maintained activity of single neurons in the cat visual cortex at different levels of retinal adaptation.

The influence of ambient illumination on the maintained electrical activity of single neurons of the cat visual cortex was studied by using the closed chamber technique for extracellular recordings. Several levels of light background within the scotopic-mesopic range were explored. Phasic and tonic changes in firing rate were observed following a background change. The former were irregular and unpredictable variations lasting up to 15-20 min. The latter, which usually followed the phasic changes, showed the constant characteristic of being in direct relation to luminance variations for neurons isolated in the striate area and in inverse relation for units recorded from the two non-striate areas of the visual cortex; in all cases, they lasted until a new luminous level was set. Changes in firing rate were not dependent upon either the neuron receptive field organization or the EEG pattern, simultaneously recorded. The background-locked firing rate variations recorded at the visual cortex seem to be the result of a particular cortical distribution of afferent fibers carrying luminance information. Applications to vision research are also suggested.

Non-oriented cells of the striate cortex activated during smooth pursuit eye movements and steady fixations in behaving monkeys.

Extracellular recordings were carried out in the primary visual cortex of behaving monkeys. Neurons were activated by moving a visual stimulus on their receptive fields during periods of steady fixation and by moving their receptive fields (smooth pursuit eye movements) on a motionless visual stimulus. Regarding non-oriented cells, they turned out to be activated by the visual stimulation both during steady fixations and smooth pursuit eye movements. Therefore, the non-oriented cells we studied seem not to receive an extraretinal signal related to the slow eye movements.

Cortical visual input to the orbito-insular cortex in the cat.

The anatomical pathways supplying the visual signal to the cat orbito-insular cortex (OIC) from primary visual areas were studied by an anterograde axonal transport technique. L-[5-3H]proline was injected, in different animals, in each of areas 17, 18, 19 and the lateral suprasylvian visual area (LS). Serial histological sections were processed by autoradiographic technique after long (8-16 days) or short (30 h) survival times. The axonal flow labelled direct pathways from LS to the ipsilateral orbital gyrus and the ventral bank of the anterior ectosylvian sulcus; this region seems to correspond to that from which many authors recorded photically evoked potentials. Long survival animals injected in LS showed labels also in the contralateral OIC. No axonal flow could be demonstrated from areas 17, 18 and 19 to OIC, either at short of long survival times. The results suggest that, apart from possible sub cortical afferences, a critical visual input may reach OIC from the extrageniculostriate visual system through LS. The functional relevance of extrastriate input to OIC is discussed.

Corticocortical connections between frontal periarcuate regions and visual areas of the superior temporal sulcus and the adjoining inferior parietal lobule in the macaque monkey.

In macaque monkeys, corticocortical connections between distinct parietotemporal visual areas (areas MST-FST, DP, and 7a) and frontal periarcuate areas are studied using tritiated aminoacids and WGA-HRP. While labeling within the banks of the principal sulcus, the dorsal part of the arcuate concavity, and the banks of the upper arcuate limb were present in both 7a and MST-FST injected animals; in the latter cases, additional projections were found towards frontal regions including the dorsomedial frontal cortex and the posterior bank of the arcuate ventral limb. Our results point to widespread frontal connections of the MST-FST complex, involving both prefrontal and premotor cortical regions.

Projections from cortical visual areas of the superior temporal sulcus to the superior colliculus, in macaque monkeys.

1. The distribution of tectal projections of two visual areas of the superior temporal sulcus (MT and MST areas) has been studied, in five Macaca fascicularis, by means of the autoradiographic method tracing the anterograde transport of tritiated aminoacids intracortically injected. 2. In all cases the ipsilateral superior colliculi (SC) were found labelled, whereas the contralateral ones were devoid of label. 3. The three brains injected in the MT area resulted in SC labels that involved the superficial gray layer (SGS), the stratum opticum (SO) and the intermediate gray layer (SGI), sparing the layers below SGI. 4. The collicular labels found after injections within the MST area exhibited their distribution over the deep SC subdivision, whereas they spared all the superficial layers but the deep part of the SO. 5. In two animals with large uptake zones, one in MT and the other in MST, the labelling within the SGI showed a cluster-like pattern. 6. The distinct found bulk of projections of MT and MST respectively to the superficial and deep subdivisions of the SC, along with a number of peculiar connections of the MST area as mentioned in the text, contribute to depict an overall neural network in which MST appears to be more strongly involved than MT in linking sensory visual with oculomotor attentive functions.

Contralateral tectal projections from single areas of the visual cortex in the cat.

1. The projections from cat cortical visuals areas to the contralateral superior colliculus (SC) were studied by the autoradiographical tracing method. Microinjections of L- [5-3H] proline were carried out in cortical visual areas 17, 18, 19 and the lateral suprasylvian visual area (LS) in different cats. Only one cortical area was injected in each animal. Survival times of 30 hours or 8 days were allowed. 2. Areas 17, 18, 19 and LS send projections to laminae, I, II and III of the frontal pole of the contralateral SC. Areas 19 and LS project also the contralateral pretectal nuclei, mainly to the posterior pretectal nucleus. 3. Cortical fibres reaching the contralateral SC pass through the brachium of the ipsilateral SC. They run along the caudal part of this structure, cross the midline and then run along the caudal part of the contralateral SC; finally, they turn anterolaterally and reach the rostal part of SC. This pathway is the tectal semidecussation (5). Cortical fibres from LS (in particular from PLLS; 15) reach the contralateral SC also via the commissure of SC. 4. Our data support the suggestion (3) that the frontal poles of SC, in the cat, may subserve straight-ahead attention and orientation to visual stimuli.

Corticopontine projections from the visual area of the superior temporal sulcus in the macaque monkey.

1. The projections from the superior temporal sulcus (STS) visual area to pontine nuclei were studied in the macaque monkey by the autoradiographic tracing method. Microinjections of a mixture of L-[5-3H] proline and L-[4,5-3H] leucine were carried out in the posterior band and the floor of the caudal half of the STS. Survival time was always 7 days. 2. The STS visual area projects to the dorsolateral part of ipsilateral pontine nuclei. Terminal projections are distributed in patches in the whole rostro-caudal extent of the pons. 3. These findings support the view that the STS visual area in the macaque monkey is homologous to the postero-medial lateral suprasylvian area in the cat.

Projections from the visual cortical region of the superior temporal sulcus to the striatum and claustrum in the macaque monkey.

Solutions of tritiated aminoacids were injected into the visual cortical region hidden in the depth of the superior temporal sulcus (STs) of the macaque monkey. Injection sites involved the middle temporal visual area, extending into the surrounding visual cortices. Projections were found homolaterally in both the striatum and claustrum. In the caudate nucleus labeled material affected mainly the body and spread both to the tail and the head of the nucleus. Label was also seen in the caudal third of the putamen and in the postero-ventral claustrum. Compared with the scarcity of afferents arising from occipital visual areas, the present data point to a heavy projection system from additional visual areas of the STs to the basal ganglia in the macaque monkey.

Projections from the cortex of the superior temporal sulcus to the dorsal lateral geniculate and pregeniculate nuclei in the macaque monkey.

Cortical projections from the visual region and adjacent polysensory region of the superior temporal sulcus (STs) to the lateral geniculate body (LGb) were investigated in the macaque monkey using an autoradiographic tracing method. Solutions of tritiated aminoacids were injected into different parts of the caudal half of the STs of five animals. A survival time of 7 days was allowed. Labels were found in both subdivisions of the LGb: the dorsal lateral geniculate nucleus (DLGn) and the pregeniculate nucleus (PGn). In particular, part of the visual cortical region adjacent to the middle temporal area (MT) projects into the DLGn as well as the PGn, whereas the MT itself and the superior temporal polysensory region project into the PGn only. Afferents to the DLGn terminate in the magnocellular layers and in their adjoining interlaminar zones, completely sparing the parvocellular layers. Afferents to the PGn terminate in separate regions of this nucleus; the MT and adjacent visual cortices project into the internal layer of the PGn, whereas the polysensosy region of the STs projects into the external retinorecipient layer of the PGn. Possible functional implications of these projections are discussed.

Effect of fast moving stimuli and saccadic eye movements on cell activity in visual areas V1 and V2 of behaving monkeys.

Extracellular recordings were carried out in the visual cortex of behaving monkeys trained on a fixation/detection task, during which a target light was displayed stationary or suddenly moving on a tangent translucent screen. The responses of visual cortical cells to fast moving stimuli during steady fixation and those obtained during rapid eye movements (saccades) which moved their receptive field across a stationary stimulus, were studied. Areas V1 and V2 were explored. When tested with rapidly moving stimuli (500 deg/sec) during steady fixation, neurons in each area behaved in almost the same way. About one fourth of them were activated, the remainder showing either no response (little more than a half of them) or a reduction of the spontaneous firing rate. In both areas, some of the neurons activated during steady fixation did not respond or responded very weakly during eye motion at saccadic velocity (500 +/- 50 deg/sec). Neurons of this type, which we refer to as 'real motion' cells, could somehow contribute to the maintenance of visual stability during the execution of large eye movements.

Autoradiographic evidence of visual cortical projections to the frontal cortex in the cat.

In II adult cats, areas 17, 18, 19 as well as the lateral suprasylvian area were separately injected with L-[5-3H] proline and their efferent projections to the frontal cortex were autoradiographically searched. Only area 19 and lateral suprasylvian area showed such projections; terminal sites were localized in the ventral and dorsal banks of the cruciate sulcus and in the adjacent mesial surface of the brain. The possibility that these labeled regions may correspond to the monkey's frontal eye field is discussed.

Optic flow direction coding in area PEc of the behaving monkey.

The cortical representation of heading perception derives from several functional processes distributed across many cortical areas. The aim of the present study was to assess if the optic flow motion directions, expansion and contraction, differently modulate the firing activity of area PEc neurons. We determined the influence of the eye position and/or the spatial position of the focus of expansion (FOE) on this activity. Single neuron activity during radial optic flow stimulation was recorded in three behaving monkeys. The retinal FOE position and the spatial eye position were examined in order to study eye position's influence upon the directional selectivity for the radial stimuli. We observed that the neurons able to discriminate the retinotopic FOE position are differently modulated by expansion and contraction. One class of neurons exhibited a different preferred FOE position during expansion and contraction. A second class showed the same preferred position with similar firing activity in the two stimuli. A third class showed the same preferred position but different firing activity. Eye position affected the directional selectivity of most PEc cells. The main result of this study is that there is a continuum in cell modulation by optic flow direction, and it can be modified by the angle of gaze with respect to the FOE. These results shed light on potential cellular integrative mechanisms of area PEc in heading perception.

Multimodal representation of optic flow in area PEc of macaque monkey.

The visual perception of self-motion is mainly provided by optic flow. Eyes usually scan the environment during locomotion, and the gaze is not always directed to the focus of expansion (FOE) of the flow field. Such eye movements change the retinal FOE position with respect to the fovea. Here, we assess if optic flow selective neurons in parietal area PEc are modulated by eye position. We recorded single neuron activity during radial optic flow stimulation in two monkeys, varying eye and retinal FOE positions. We found that the majority of PEc neurons are modulated by the FOE retinotopic position with different tuning for expansion and contraction. Although many neurons did not show any gaze field without visual stimulation, the eye position modulated optic flow responses in about half of the cells. These novel results suggest that PEc neurons integrate both visual and eye position signals, and allow us to hypothesize their role in guiding locomotion as a part of a cortical network involved in FOE representation during self-motion. Visual and eye position interaction in this area could be seen as a contribution to the building of the invariant space representation necessary to motor planning.