Milena Raffi

A functional architecture of optic flow in the inferior parietal lobule of the behaving monkey.

The representation of navigational optic flow across the inferior parietal lobule was assessed using optical imaging of intrinsic signals in behaving monkeys. The exposed cortex, corresponding to the dorsal-most portion of areas 7a and dorsal prelunate (DP), was imaged in two hemispheres of two rhesus monkeys. The monkeys actively attended to changes in motion stimuli while fixating. Radial expansion and contraction, and rotation clockwise and counter-clockwise optic flow stimuli were presented concentric to the fixation point at two angles of gaze to assess the interrelationship between the eye position and optic flow signal. The cortical response depended upon the type of flow and was modulated by eye position. The optic flow selectivity was embedded in a patchy architecture within the gain field architecture. All four optic flow stimuli tested were represented in areas 7a and DP. The location of the patches varied across days. However the spatial periodicity of the patches remained constant across days at ∼950 and 1100 µm for the two animals examined. These optical recordings agree with previous electrophysiological studies of area 7a, and provide new evidence for flow selectivity in DP and a fine scale description of its cortical topography. That the functional architectures for optic flow can change over time was unexpected. These and earlier results also from inferior parietal lobule support the inclusion of both static and dynamic functional architectures that define association cortical areas and ultimately support complex cognitive function.

Multiple cortical representations of optic flow processing

When an observer moves through the environment, moving images form on his or her retinae. The visual perception of self-motion is provided by expanding or contracting visual fields projected on the retina. Gibson (1950) called this particular motion, originated by the observer’s own navigation, “Optic Flow”. He noted that when an observer moves forward, fixating his or her final destination, the expanding visual field seems to originate from a specific point and he named this point “Focus of Expansion” (FOE). In everyday life, self-motion perception is more complicated, because eye and vestibular movements almost always occur together with the optic flow. For example, during locomotion, we experience retinal flow, composed of the translational and rotational components of eye, head and body movements, and optic flow (Lappe et al., 1999). Although all the self–motion perception mechanisms are not clear yet, it seems that the visual system analyzes the visual component, i.e. the optic flow, first and then it combines the optic flow with the other retinal and extraretinal signals in order to construct a dynamic map of extrapersonal space suitable for self–motion guidance (Regan & Beverley, 1982; Warren & Hannon, 1990; Lappe et al., 1999).

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.

Effect of early isolation on signal transfer in the entorhinal cortex–dentate–hippocampal system

Deprivation of socio-sensory interactions during early life impairs brain function in adulthood. In previous investigations we showed that early isolation severely affects neuron development in several structures of the hippocampal region, including the entorhinal cortex. In the present study we investigated the effects of early isolation on signal processing along the entorhinal cortex-dentate-CA3-CA1 system, a major memory circuit of the hippocampal region. Male and female guinea-pigs were assigned at 6-7 days of age to either a social or an isolated environment. At 90-100 days of age the animals were anesthetized and field potentials were recorded from the entorhinal cortex-dentate-CA3-CA1 circuit, driven by dorsal psalterium commissural volleys. Analysis of the input-output function in the different structures showed that in isolated males there was a small reduction in the input-output function of the population excitatory postsynaptic potential and population spike evoked in layer II of the entorhinal cortex. No changes occurred in isolated females. In isolated males and females there was a reduction in the input-output function of the population excitatory postsynaptic potential and population spike evoked in the dentate gyrus, CA3 and CA1, but this effect was larger in males. In isolated males, but not in females, the population spike/population excitatory postsynaptic potential ratio was reduced in all investigated structures, indicating that in males the size of the discharged neuron population was reduced more than due to the decreased input. Results show that isolation reduces the synaptic function in the whole entorhinal cortex-dentate gyrus-CA3-CA1 system. While the entorhinal cortex was moderately impaired, the dentate-hippocampal system was more severely affected. The impairment in the signal transfer along the entorhinal cortex-dentate gyrus-CA3-CA1 system was heavier in males, confirming the larger susceptibility of this sex to early experience. This work provides evidence that malfunctioning of a major hippocampal network may underlie the learning deficits induced by impoverished surroundings during early life.

Importance of optic flow for postural stability of male and female young adults

PurposeA feedback control process based on self-motion perception contributes to postural stability; however, little is known about the visual modulation of postural muscles. The aim of this study was to investigate the effect of optic flow stimuli, presented full field, in the peripheral and foveal visual field, on muscular activation. Then, we assessed the correlation between optic flow, muscle activity and body sway in male and female subjects.MethodsWe used surface electromyography (EMG) and stabilometry on 24 right-handed young adults. We recorded the bilateral activation of tibialis anterior, gastrocnemius medialis, biceps femoris and vastus medialis. EMG and center of pressure (COP) signals were acquired simultaneously. EMG signal amplitude was computed as root mean square normalized by baseline.ResultsWe found a significant effect for muscles, gender and an interaction effect of muscle by gender (ANOVA, pxa0<xa00.001). Results showed different postural alignments in males and females. The COP spatial variability during peripheral stimuli was generally reduced. The prevalent direction of oscillation evoked by peripheral stimuli was clustered, while foveal and random stimuli induced distributed and randomized directions. Also for muscle activity, we found gender differences in the prevalent oscillation distributions evoked by optic flow.ConclusionVisual stimuli always evoke an excitatory input on postural muscles, but the stimulus structure produces different postural effects. Peripheral optic flow stimuli stabilize postural sway, while random and foveal optic flow provoke larger sway variability similar to those evoked in the absence of visual stimulation.

Gaze and smooth pursuit signals interact in parietal area 7m of the behaving monkey.

Posterior parietal cortex is a region specialized for multimodal integration and coordinate transformations which converts sensory input to motor output. Eye position signals are crucial for such transformations, because they are needed to the inner reconstruction of a stable image of the outside world in spite of eye movements. Area 7m is a parietal area anatomically connected with oculomotor structures such as frontal eye field and superior colliculus. The aim of this study was to assess if neurons in area 7m possess activity related to eye movements, and if so, which sort of movements are processed. We recorded the extracellular activity of 7m neurons in two monkeys trained in both a smooth pursuit and a visually guided saccade task. The majority of neurons tested with the smooth pursuit task (16/17) showed directional selectivity influenced by the eye position. Moreover, these neurons were tuned to inward or outward pursuit with respect to the center of extra-personal visual space. About half of the cells (11/24) tested with the saccade task changed their activity during the pre-saccadic period. The majority of neurons presented post-saccadic activity: most of the cells showed a directionally-selective phasic response and a modulation by eye position during fixation (23/24). Overall, we observed that area 7m contains a population of neurons signaling smooth pursuit direction at certain eye position and saccade direction toward specific portions of the visual space. We hypothesize that area 7m might be involved in spatial map updating which can be used for spatial orientation.

Effects of early isolation on layer II neurons in the entorhinal cortex of the guinea pig.

Previous studies showed that early environmental conditions severely affect the morphology of the granule cells in the hippocampal dentate gyrus and pyramidal neurons in fields CA3 and CA1. The aim of the present study was to determine whether early isolation affects neuron morphology in layer II of the entorhinal cortex, from which the perforant path to the dentate gyrus and CA3 takes its origin. Male and female guinea pigs were assigned at 6-7 days of age to either a control (social) or an isolated environment where they remained for 80-90 days. The brains were Golgi-Cox stained and neurons were sampled from layer II of the entorhinal cortex. Morphometric analysis was carried out on star cells, the most abundant neuron population. Isolated males had star cells with less dendritic branches, a shorter dendritic length and a smaller dendritic spine density than control males. In contrast, isolated females had more dendritic branches than control females, though this difference was of small magnitude. While isolated males had star cells with a smaller soma than control males, isolated females had a soma larger than control females. In both environments sex differences were found in the star cell morphology. In the control environment males had more dendritic branches, a greater dendritic length, a larger soma but a smaller spine density than females. In the isolated environment males had less branches, a shorter dendritic length, a smaller spine density and a smaller soma than females. The results indicate that early isolation affects the structure of the star cells in the entorhinal cortex and that males and females react to isolation in an opposite manner. A similar sexually dimorphic response to early isolation was previously observed in the dentate gyrus and fields CA3 and CA1. The presence of widespread effects of isolation in the entorhinal cortex and numerous hippocampal structures suggests that the outcome of early isolation might be a change in learning and memory functions requiring the hippocampal region.

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.

Optic flow neurons in area PEc integrate eye and head position signals.

Neurons in area PEc, a visual area located in the superior parietal lobule, are activated by optic flow stimuli. An important issue is whether PEc neurons are able to integrate multimodal signals, such as those related to optic flow selectivity with those about eye and head position. The aim of this study was to assess if angle of gaze and/or head rotation modify the spatial representation of the focus of expansion (FOE), varying FOE, fixation point and head position in space. We found that the rotation of head modulated the firing activity of PEc optic flow neurons. The head position also changed the angle of gaze effect on the PEc neuronal activity. All recorded neurons showed a main interaction effect between head and eye position upon the selectivity for optic flow stimuli. These results seem to suggest that PEc optic flow neurons use different reference frames depending on the position of the eye and/or the head in space emphasizing a possible contribution of this area in guiding locomotion by integrating multiple extraretinal inputs.

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 positions 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.