Shifting receptive fields.

The very notion of a receptive field implies a defined, static region of sensitivity—for visual neurons, a region in retinotopic space. Other factors besides retinal stimulation (such as attentional state) may modulate neural responses, but the shape and position of the receptive field should remain fixed, permanently constrained by anatomical connectivity.Not so, as it turns out, for some visual neurons. For example, Goldberg and colleagues presented evidence for “predictive remapping” of visual receptive fields in the lateral intraparietal area (LIP) (Duhamel et al., 1992xDuhamel, J.-R., Colby, C.L., and Goldberg, M.E. Science. 1992; 255: 90–92Crossref | PubMedSee all References(Duhamel et al., 1992), a part of macaque visual cortex thought to play a role in saccadic eye movements. For many LIP cells, immediately prior to a saccadic eye movement, the receptive field seems to shift temporarily across the retina in the same direction as the intended saccade. The result of this anticipatory shift is that the cell responds to stimuli that appear in its ultimate receptive field location before the eyes have even moved. This neural phenomenon may help to maintain a stable representation of the world in spite of the constant shifts in the retinal image produced by eye movements.Not just eye movements, but body movements as well can alter visual receptive field positions. Gross and colleagues have studied visually sensitive neurons in macaque ventral premotor cortex, which is involved in controlling body movements. Most of these neurons are bimodal—they respond to both visual and tactile stimulation. Frequently, the visual and tactile receptive fields are related. For example, a neuron with a tactile receptive field near the mouth will also respond to visual stimuli near the mouth. Graziano, Yap, and Gross (1994)xGraziano, M.S., Yap, G.S., and Gross, C.G. Science. 1994; 266: 1054–1057Crossref | PubMedSee all ReferencesGraziano, Yap, and Gross (1994) studied cells with bimodal receptive fields associated with the arm and showed that, when arm position changed, visual receptive fields typically shifted across the retina in the same direction as the arm. They proposed that these cells encode visual (and tactile) stimuli in an arm-centered coordinate system, in order to facilitate sensory guidance of arm movements.These previous reports of receptive field shifts associated with eye and body movements have involved brain structures implicated in controlling or representing such movements. But in the current issue of Neuron, Tolias et al. (2001)xTolias, A.S., Moore, T., Smirnakis, S.M., Tehovnik, E.J., Siapas, A.G., and Schiller, P.H. Neuron. 2001; 29: 757–767Abstract | Full Text | Full Text PDF | PubMed | Scopus (156)See all ReferencesTolias et al. (2001) demonstrate eye movement–related receptive field shifts in macaque area V4, part of the ventral pathway of visual cortex, which is responsible for object recognition. In their experiment, each trial begins with the monkey fixating on a small target. Then a probe stimulus, customized to evoke responses from the V4 cell being studied, appears in or near the receptive field and remains present throughout the rest of the trial. Finally, the fixation target disappears and a small saccade target appears elsewhere on the screen, and the monkey is rewarded for saccading to the target. The response region of the cell is mapped by varying the probe location from trial to trial. The saccade target location is also varied.The critical result is that for many V4 cells the receptive field seems to shift toward the saccade target around the time of the saccade. The receptive field during this perisaccadic period is defined by a burst of renewed activity associated with the saccade. Such perisaccadic activation of V4 responses has previously been demonstrated in experiments where the probe stimulus itself was the saccade target (Fischer and Boch 1981xFischer, B. and Boch, R. Exp. Brain Res. 1981; 44: 129–137Crossref | PubMed | Scopus (93)See all References, Moore et al. 1998xMoore, T., Tolias, A.S., and Schiller, P.H. Proc. Natl. Acad. Sci. USA. 1998; 95: 8981–8984Crossref | PubMed | Scopus (67)See all References). In the current experiment, the probe and saccade target are dissociated so that the probe can be used to map the spatial distribution of the reactivation. In many instances, the perisaccadic receptive field is shifted (toward the saccade target) relative to the classical receptive field (defined by responses to probe onsets, which occur earlier in the behavioral trials). The shifts appear moderate in size—on the order of one receptive field diameter or less—in contrast to the large-scale remappings observed in LIP and ventral premotor cortex. The perisaccadic receptive fields tend to be smaller than the classical receptive fields, though this may just reflect weaker activity relative to the probe onset responses.The authors advance two interpretations of the receptive field shifts. First, they suggest that presaccadic activity in V4 may contribute to selection of the next saccade target. Under natural viewing conditions, saccade endpoints correspond to salient and informative features in the visual image. Selection of these features presumably depends on object processing in the ventral pathway. Presaccadic receptive field shifts could enhance processing near the future saccade endpoint and thus facilitate target selection. However, the relatively brief latency between perisaccadic reactivation and saccade initiation (an average of 26 ms in this study) raises the question of whether there is time for this activity to influence the upcoming saccade. Perhaps under natural viewing conditions, with leisurely, voluntary selection of saccade targets, perisaccadic V4 activity would begin earlier relative to saccade onset.Second, the authors suggest that receptive field shifts toward the saccade target may accelerate processing of stimuli near the upcoming region of fixation. In support, they cite psychophysical results showing enhanced visual perception near saccade targets prior to saccade initiation (Hoffman and Subramaniam 1995xPercept. Hoffman, J.E. and Subramaniam, B. Psychophys. 1995; 57: 787–795Crossref | Scopus (743)See all References, Kowler et al. 1995xKowler, E., Anderson, E., Dosher, B., and Blaser, E. Vision Res. 1995; 35: 1897–1916Crossref | PubMed | Scopus (704)See all References). As Tolias et al. note, this presaccadic perceptual enhancement is thought to reflect a preliminary shift in attention associated with saccades.A relationship to attention seems particularly likely, since similar V4 receptive field shifts, associated not with eye movements but with movements of the attentional focus, have previously been described by Van Essen and colleagues (Connor et al., 1997xConnor, C.E., Preddie, D.C., Gallant, J.L., and Van Essen, D.C. J. Neurosci. 1997; 17: 3201–3214PubMedSee all References(Connor et al., 1997). In their experiment, the monkey maintained fixation at a single point throughout the trial, but attended to one out of an array of target stimuli surrounding the receptive field. While the monkey performed this peripheral attention task, probe stimuli were flashed at various positions in and near the V4 receptive field to generate a response map. Receptive field maps were obtained for multiple attention target positions.In the Van Essen experiment, many V4 cells exhibited a receptive field shift toward the attention target, much like the shifts toward saccade targets reported by Tolias et al. This suggests that the same attention-related mechanisms may have been operative in both experiments. In addition, for the majority of V4 cells in the Van Essen study, overall response level depended strongly on the direction of the attentional focus relative to the receptive field. A given cell might respond briskly (to probe stimuli flashed in the receptive field) when attention was directed to the right of the receptive field, but remain silent when attention was directed to the left. Tolias et al. may have observed a similar phenomenon, since only certain saccade target positions evoked perisaccadic activation for any given cell. The mechanistic implications of receptive field shifts and attention direction tuning have been discussed elsewhere (Moran and Desimone 1985xMoran, J. and Desimone, R. Science. 1985; 229: 782–784Crossref | PubMedSee all References, Olshausen et al. 1993xOlshausen, B.A., Anderson, C.H., and Van Essen, D.C. J. Neurosci. 1993; 13: 4700–4719PubMedSee all References, Connor et al. 1997xConnor, C.E., Preddie, D.C., Gallant, J.L., and Van Essen, D.C. J. Neurosci. 1997; 17: 3201–3214PubMedSee all References, Salinas and Abbott 1997xSalinas, E. and Abbott, L.F. J. Neurophysiol. 1997; 77: 3267–3272PubMedSee all References).The emerging scientific picture thus confirms one's subjective impression that saccadic eye movements and shifts of attention are closely linked. Most eye movements are preceded by attentional shifts, and, under normal conditions, most attentional shifts are succeeded by eye movements. The preceding attentional shift facilitates visual processing at the saccade target location, perhaps aiding in target selection and accelerating perception of the new item of interest. The early attention shift has previously been measured at the psychological level in terms of enhanced perceptual performance near the saccade target. Now Tolias et al. appear to have observed this attentional shift at the neural level, by demonstrating a signature response change (receptive field shifts) known to be associated with attention. This convergence between psychological and neurophysiological evidence provides compelling evidence for the close relationship between eye movements and attentional shifts.