Visuomotor control in mice and primates.

We conduct a comparative evaluation of the visual systems from the retina to the muscles of the mouse and the macaque monkey noting the differences and similarities between these two species. The topics covered include (1) visual-field overlap, (2) visual spatial resolution, (3) V1 cortical point-image [i.e., V1 tissue dedicated to analyzing a unit receptive field], (4) object versus motion encoding, (5) oculomotor range, (6) eye, head, and body movement coordination, and (7) neocortical and cerebellar function. We also discuss blindsight in rodents and primates which provides insights on how the neocortex mediates conscious vision in these species. This review is timely because the field of visuomotor neurophysiology is expanding beyond the macaque monkey to include the mouse; there is therefore a need for a comparative analysis between these two species on how the brain generates visuomotor responses.

Direct and indirect activation of cortical neurons by electrical microstimulation.

Electrical microstimulation has been used to elucidate cortical function. This review discusses neuronal excitability and effective current spread estimated by using three different methods: 1) single-cell recording, 2) behavioral methods, and 3) functional magnetic resonance imaging (fMRI). The excitability properties of the stimulated elements in neocortex obtained using these methods were found to be comparable. These properties suggested that microstimulation activates the most excitable elements in cortex, that is, by and large the fibers of the pyramidal cells. Effective current spread within neocortex was found to be greater when measured with fMRI compared with measures based on single-cell recording or behavioral methods. The spread of activity based on behavioral methods is in close agreement with the spread based on the direct activation of neurons (as opposed to those activated synaptically). We argue that the greater activation with imaging is attributed to transynaptic spread, which includes subthreshold activation of sites connected to the site of stimulation. The definition of effective current spread therefore depends on the neural event being measured.

Motion processing in the macaque: revisited with functional magnetic resonance imaging.

A great deal is known about the response properties of single neurons processing sensory information. In contrast, less is understood about the collective characteristics of networks of neurons that may underlie sensory capacities of animals. We used functional magnetic resonance imaging to study the emergent properties of populations of neurons processing motion across different brain areas. Using a visual adaptation paradigm, we localized a distributed network of visual areas that process information about the direction of motion as expected from single-cell recording studies. However, we found an apparent discrepancy between the directional signals in certain visual areas as measured with blood oxygenation level-dependent imaging compared with an estimate based on the spiking of single neurons. We propose a hypothesis that may account for this difference based on the postulate that neuronal selectivity is a function of the state of adaptation. Consequently, neurons classically thought to lack information about certain attributes of the visual scene may nevertheless receive and process this information. We further hypothesize that this adaptation-dependent selectivity may arise from intra- or inter-area cellular connections, such as feedback from higher areas. This network property may be a universal principle the computational goal of which is to enhance the ability of neurons in earlier visual areas to adapt to statistical regularities of the input and therefore increase their sensitivity to detect changes along these stimulus dimensions.

Eye movements modulate visual receptive fields of V4 neurons.

The receptive field, defined as the spatiotemporal selectivity of neurons to sensory stimuli, is central to our understanding of the neuronal mechanisms of perception. However, despite the fact that eye movements are critical during normal vision, the influence of eye movements on the structure of receptive fields has never been characterized. Here, we map the receptive fields of macaque area V4 neurons during saccadic eye movements and find that receptive fields are remarkably dynamic. Specifically, before the initiation of a saccadic eye movement, receptive fields shrink and shift towards the saccade target. These spatiotemporal dynamics may enhance information processing of relevant stimuli during the scanning of a visual scene, thereby assisting the selection of saccade targets and accelerating the analysis of the visual scene during free viewing.

Visual representations during saccadic eye movements.

In normal vision, shifts of attention are usually followed by saccadic eye movements. Neurons in extrastriate area V4 are modulated by focal attention when eye movements are withheld, but they also respond in advance of visually guided saccadic eye movements. We have examined the visual selectivity of saccade-related responses of area V4 neurons in monkeys making delayed eye movements to receptive field stimuli of varying orientation. This task did not require the monkey to attend to orientation per se but merely to foveate the receptive field stimulus. We present evidence that the presaccadic enhancement exhibited by V4 neurons, quite separate from the response at stimulus onset, is a resurgent visual representation that seems as selective as the response is when the stimulus first appears. The presaccadic enhancement appears to provide a strengthening of a decaying featural representation immediately before an eye movement is directed to visual targets. We suggest that this reactivation provides a mechanism by which a clear perception of the saccade goal can be maintained during the execution of the saccade, perhaps for the purpose of establishing continuity across eye movements.

Saccades induced electrically from the dorsomedial frontal cortex: evidence for a head-centered representation.

The amplitude and direction of saccadic eye movements evoked electrically from the dorsomedial frontal cortex (DMFC) of monkeys vary with starting eye position. This observation has been used to argue that the DMFC codes saccadic eye movements in head-centered coordinates. Whether the amplitude and direction of the evoked saccades are also affected by changes in head position has never been demonstrated. Such a result would argue against a head-centered representation, and instead would suggest a representation anchored to another body part. Tests were conducted on rhesus monkeys to determine whether changing the position of the head with respect to the trunk or changing the position of the head with respect to the gravitational axis alters saccadic parameters. The amplitude and direction of saccadic eye movements remained invariant to such manipulations. These findings confirm the claim that the DMFC encodes saccadic eye movements in head-centered coordinates.

Colour adaptation modifies the long-wave versus middle-wave cone weights and temporal phases in human luminance (but not red-green) mechanism.

1. The human luminance (LUM) mechanism detects rapid flicker and motion, responding to a linear sum of contrast signals, L' and M', from the long-wave (L) and middle-wave (M) cones. The red-green mechanism detects hue variations, responding to a linear difference of L' and M' contrast signals. 2. The two detection mechanisms were isolated to assess how chromatic adaptation affects summation of L' and M' signals in each mechanism. On coloured background (from blue to red), we measured, as a function of temporal frequency, both the relative temporal phase of the L' and M' signals producing optimal summation and the relative L' and M' contrast weights of the signals (at the optimal phase for summation). 3. Within the red-green mechanism at 6 Hz, the phase shift between the L' and M' signals was negligible on each coloured field, and the L' and M' contrast weights were equal and of opposite sign. 4. Relative phase shifts between the L' and M' signals in the LUM mechanism were markedly affected by adapting field colour. For stimuli of 1 cycle deg-1 and 9 Hz, the temporal phase shift was zero on a green-yellow field (approximately 570 nm). On an orange field, the L' signal lagged M' by as much as 70 deg phase while on a green field M' lagged L' by as much as 70 deg. The asymmetric phase shift about yellow adaptation reveals a spectrally opponent process which controls the phase shift. The phase shift occurs at an early site, for colour adaptation of the other eye had no effect, and the phase shift measured monocularly was identical for flicker and motion, thus occurring before the motion signal is extracted (this requires an extra delay). 5. The L' versus M' phase shift in the LUM mechanism was generally greatest at intermediate temporal frequencies (4-12 Hz) and was small at high frequencies (20-25 Hz). The phase shift was greatest at low spatial frequencies and strongly reduced at high spatial frequencies (5 cycle deg-1), indicating that the receptive field surround of neurones is important for the phase shift. 6. These temporal phase shifts were confirmed by measuring motion contrast thresholds for drifting L cone and M cone gratings summed in different spatial phases. Owing to the large phase shifts on green or orange fields, the L and M components were detected about equally well by the LUM mechanism (at 1 cycle deg-1 and 9 Hz) when summed spatially in phase or in antiphase. Antiphase summation is typically thought to produce an equiluminant red-green grating. 7. At low spatial frequency, the relative L' and M' contrast weights in the LUM mechanism (assessed at the optimal phase for summation) changed strongly with field colour and temporal frequency. 8. The phase shifts and changing contrast weights were modelled with phasic retinal ganglion cells, with chromatic adaptation strongly modifying the receptive field surround. The cells summate L' and M' in their centre, while the surround L' and M' signals are both antagonistic to the centre for approximately 570 nm yellow adaptation. Green or orange adaptation is assumed to modify the L and M surround inputs, causing them to be opponent with respect to each other, but with reversed polarity on the green versus orange field (to explain the chromatic reversal of the phase shift). Large changes in the relative L' and M' weights on green versus orange fields indicate the clear presence of the spectrally opponent surround even at 20 Hz. The spectrally opponent surround appears sluggish, with a long delay (approximately 20 ms) relative to the centre.