Spatial determinants of multisensory integration in cat superior colliculus neurons

1996 ◽  
Vol 75 (5) ◽  
pp. 1843-1857 ◽  
Author(s):  
M. A. Meredith ◽  
B. E. Stein

1. Although a representation of multisensory space is contained in the superior colliculus, little is known about the spatial requirements of multisensory stimuli that influence the activity of neurons here. Critical to this problem is an assessment of the registry of the different receptive fields within individual multisensory neurons. The present study was initiated to determine how closely the receptive fields of individual multisensory neurons are aligned, the physiological role of that alignment, and the possible functional consequences of inducing receptive-field misalignment. 2. Individual multisensory neurons in the superior colliculus of anesthetized, paralyzed cats were studied with the use of standard extracellular recording techniques. The receptive fields of multisensory neurons were large, as reported previously, but exhibited a surprisingly high degree of spatial coincidence. The average proportion of receptive-field overlap was 86% for the population of visual-auditory neurons sampled. 3. Because of this high degree of intersensory receptive-field correspondence, combined-modality stimuli that were coincident in space tended to fall within the excitatory regions of the receptive fields involved. The result was a significantly enhanced neuronal response in 88% of the multisensory neurons studied. If stimuli were spatially disparate, so that one fell outside its receptive field, either a decreased response occurred (56%), or no intersensory effect was apparent (44%). 4. The normal alignment of the different receptive fields of a multisensory neuron could be disrupted by passively displacing the eyes, pinnae, or limbs/body. In no case was a shift in location or size observed in a neuron's other receptive field(s) to compensate for this displacement. The physiological result of receptive-field misalignment was predictable and based on the location of the stimuli relative to the new positions of their respective receptive fields. Now, for example, one component of a spatially coincident pair of stimuli might fall outside its receptive field and inhibit the other's effects. 5. These data underscore the dependence of multisensory integrative responses on the relationship of the different stimuli to their corresponding receptive fields rather than to the spatial relationship of the stimuli to one another. Apparently, the alignment of different receptive fields for individual multisensory neurons ensures that responses to combinations of stimuli derived from the same event are integrated to increase the salience of that event. Therefore the maintenance of receptive-field alignment is critical for the appropriate integration of converging sensory signals and, ultimately, elicitation of adaptive behaviors.

2011 ◽  
Vol 106 (4) ◽  
pp. 1862-1874 ◽  
Author(s):  
Jan Churan ◽  
Daniel Guitton ◽  
Christopher C. Pack

Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.


2017 ◽  
Author(s):  
V. C. Caruso ◽  
D. S. Pages ◽  
M. A. Sommer ◽  
J. M. Groh

ABSTRACTWe accurately perceive the visual scene despite moving our eyes ~3 times per second, an ability that requires incorporation of eye position and retinal information. We assessed how this neural computation unfolds across three interconnected structures: frontal eye fields (FEF), intraparietal cortex (LIP/MIP), and the superior colliculus (SC). Single unit activity was assessed in head-restrained monkeys performing visually-guided saccades from different initial fixations. As previously shown, the receptive fields of most LIP/MIP neurons shifted to novel positions on the retina for each eye position, and these locations were not clearly related to each other in either eye- or head-centered coordinates (hybrid coordinates). In contrast, the receptive fields of most SC neurons were stable in eye-centered coordinates. In FEF, visual signals were intermediate between those patterns: around 60% were eye-centered, whereas the remainder showed changes in receptive field location, boundaries, or responsiveness that rendered the response patterns hybrid or occasionally head-centered. These results suggest that FEF may act as a transitional step in an evolution of coordinates between LIP/MIP and SC. The persistence across cortical areas of hybrid representations that do not provide unequivocal location labels in a consistent reference frame has implications for how these representations must be read-out.New & NoteworthyHow we perceive the world as stable using mobile retinas is poorly understood. We compared the stability of visual receptive fields across different fixation positions in three visuomotor regions. Irregular changes in receptive field position were ubiquitous in intraparietal cortex, evident but less common in the frontal eye fields, and negligible in the superior colliculus (SC), where receptive fields shifted reliably across fixations. Only the SC provides a stable labelled-line code for stimuli across saccades.


1978 ◽  
Vol 41 (2) ◽  
pp. 285-304 ◽  
Author(s):  
A. Antonini ◽  
G. Berlucchi ◽  
J. M. Sprague

1. In agreement with previous work, we have found that the ipsilateral visual field is represented in an extensive rostral portion--from one-third to one-half--of the superior colliculus (SC) of the cat. This representation is binocular. The SC representation of the ipsilateral visual field can be mediated both directly, by crossed retinotectal connections originating from temporal hemiretina, and indirectly, by across-the-midline connections relaying visual information from one-half of the brain to contralateral SC. 2. In order to study the indirect, across-the-midline visual input to the SC, we have recorded responses of SC neurons to visual stimuli presented to either the ipsilateral or the contralateral eye of cats with a midsagittal splitting of the optic chiasm. Units driven by the ipsilateral eye, presumably through the direct retinotectal input and/or corticotectal connections from ipsilateral visual cortex, were found throughout the SC, except at its caudal pole, which normally receives fibers from the extreme periphery of the contralateral nasal hemiretina. Units driven by the contralateral eye, undoubtedly through an indirect across-the-midline connection, were found only in the anterior portion of the SC, in which is normally represented the ipsilateral visual field. Receptive fields in both ipsilateral and contralateral eye had properties typical of SC receptive fields in cats with intact optic pathways. 3. All units having a receptive field in the contralateral eye had also a receptive field in the ipsilateral eye; for each of these units, the receptive fields in both eyes invariably abutted the vertical meridian of the visual field. The receptive field in one eye had about the same elevation relative to the horizontal meridian and the same vertical extension as the receptive field in the other eye; the two receptive fields of each binocular unit matched each other at the vertical meridian and formed a combined receptive field straddling the vertical midline of the horopter...


1982 ◽  
Vol 47 (2) ◽  
pp. 272-286 ◽  
Author(s):  
J. Graham ◽  
N. Berman ◽  
E. H. Murphy

1. One hundred seventy-nine single units were studied in the superior colliculus of seven Dutch-belted rabbits following ablation of the ipsilateral visual cortex. The response characteristics of these units were compared with those of 284 single units recorded from the superior colliculus of 20 intact animals. 2. In both the upper and lower parts of the stratum griseum superficiale and in the stratum griseum intermediate, there were smaller proportions of direction-selective visual units in the decorticated animals than in normal ones. 3. In the upper stratum griseum superficiale, a larger proportion of units responded to stroboscopic illumination in the decorticated animals than in normal ones. Also, in the decorticated animals, there was a larger proportion of units whose responses to a small moving stimulus were inhibited by the simultaneous presentation of stroboscopic illumination. 4. In both the upper and lower parts of the stratum griseum superficiale, a larger proportion of visual units responded well to stationary stimuli and a smaller proportion of visual units showed habituation in decorticated animals compared to normal ones. 5. In the lower stratum griseum superficiale, the receptive fields of units were larger and were more elongated in the anterior-posterior dimension in the decorticated animals than in normal ones. 6. In the two preparations, units did not differ in responsiveness or spontaneous activity; and visual units did not differ in the sustained or transient nature of their responses, the selectivity for light or dark stimuli, the selectivity for onset or offset of the stimuli, or the selectivity for stimulus velocity. 7. This study provides evidence for the importance of the visual corticotectal projection in the elaboration of the visual receptive-field properties of units in the superior colliculus of the rabbit. In addition, this study shows that the subdivisions of the superior colliculus are differentially affected by the loss of the visual corticotectal projection.


1978 ◽  
Vol 41 (6) ◽  
pp. 1359-1372 ◽  
Author(s):  
P. C. Fox ◽  
K. L. Chow ◽  
A. S. Kelly

1. The receptive-field characteristics of superior colliculus neurons were studied in rabbit pups that had one eyelid sutured prior to eye opening. Units recorded from the superior colliculus (SC) receiving input from the unsutured eye provided normal developmental data, and those from the colliculus receiving input from the sutured eye were used to study the effect of visual deprivation. 2. A total of 1,054 cells recorded from 89 animals ranging in age from 7 to 35 days were obtained, 514 cells in the normal colliculus and 540 cells in the deprived colliculus. During normal development, three nonoriented cell types (concentric, uniform, motion) showed a progressive increase in relative frequency of occurrence, starting at about 7 days and reaching the adult level at about 15 days. Directionally selective cells developed slightly later, reaching an adult level at 3 wk. Oriented directional cells were the slowest to mature, requiring about 4 wk to reach the final level. 3. Eyelid suturing significantly affected the oriented directional cell development; these cells developed at a normal rate for about 3 wk, then rather abruptly began to decrease in number; a stable relative frequency of about one-fourth the normal value was reached at about 4 wk. A corresponding increase in the relative number of indefinite cells to above the normal level also occurred. In contrast, the development of nonoriented cells and directionally selective cells was not affected by the deprivation. 4. The development of rabbit superior colliculus receptive fields was found to be, in general, similar to development of kitten SC receptive fields. It also correlates well with developmental changes seen in rabbit ganglion cell receptive fields and with anatomical changes in developing rabbit SC. Indirect support is given for the hypothesis that changes seen in SC with deprivation are secondary to changes in the visual cortex.


1995 ◽  
Vol 73 (5) ◽  
pp. 1988-2003 ◽  
Author(s):  
M. F. Walker ◽  
E. J. Fitzgibbon ◽  
M. E. Goldberg

1. Previous experiments have shown that visual neurons in the lateral intraparietal area (LIP) respond predictively to stimuli outside their classical receptive fields when an impending saccade will bring those stimuli into their receptive fields. Because LIP projects strongly to the intermediate layers of the superior colliculus, we sought to demonstrate similar predictive responses in the monkey colliculus. 2. We studied the behavior of 90 visually responsive neurons in the superficial and intermediate layers of the superior colliculus of two rhesus monkeys (Macaca mulatta) when visual stimuli or the locations of remembered stimuli were brought into their receptive fields by a saccade. 3. Thirty percent (18/60) of intermediate layer visuomovement cells responded predictively before a saccade outside the movement field of the neuron when that saccade would bring the location of a stimulus into the receptive field. Each of these neurons did not respond to the stimulus unless an eye movement brought it into its receptive field, nor did it discharge in association with the eye movement unless it brought a stimulus into its receptive field. 4. These neurons were located in the deeper parts of the intermediate layers and had relatively larger receptive fields and movement fields than the cells at the top of the intermediate layers. 5. The predictive responses of most of these neurons (16/18, 89%) did not require that the stimulus be relevant to the monkey's rewarded behavior. However, for some neurons the predictive response was enhanced when the stimulus was the target of a subsequent saccade into the neuron's movement field. 6. Most neurons with predictive responses responded with a similar magnitude and latency to a continuous stimulus that remained on after the saccade, and to the same stimulus when it was only flashed for 50 ms coincident with the onset of the saccade target and thus never appeared within the cell's classical receptive field. 7. The visual response of neurons in the intermediate layers of the colliculus is suppressed during the saccade itself. Neurons that showed predictive responses began to discharge before the saccade, were suppressed during the saccade, and usually resumed discharging after the saccade. 8. Three neurons in the intermediate layers responded tonically from stimulus appearance to saccade without a presaccadic burst. These neurons responded predictively to a stimulus that was going to be the target for a second saccade, but not to an irrelevant flashed stimulus. 9. No superficial layer neuron (0/27) responded predictively when a stimulus would not be brought into their receptive fields by a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)


2018 ◽  
Vol 119 (4) ◽  
pp. 1411-1421 ◽  
Author(s):  
Valeria C. Caruso ◽  
Daniel S. Pages ◽  
Marc A. Sommer ◽  
Jennifer M. Groh

We accurately perceive the visual scene despite moving our eyes ~3 times per second, an ability that requires incorporation of eye position and retinal information. In this study, we assessed how this neural computation unfolds across three interconnected structures: frontal eye fields (FEF), intraparietal cortex (LIP/MIP), and the superior colliculus (SC). Single-unit activity was assessed in head-restrained monkeys performing visually guided saccades from different initial fixations. As previously shown, the receptive fields of most LIP/MIP neurons shifted to novel positions on the retina for each eye position, and these locations were not clearly related to each other in either eye- or head-centered coordinates (defined as hybrid coordinates). In contrast, the receptive fields of most SC neurons were stable in eye-centered coordinates. In FEF, visual signals were intermediate between those patterns: around 60% were eye-centered, whereas the remainder showed changes in receptive field location, boundaries, or responsiveness that rendered the response patterns hybrid or occasionally head-centered. These results suggest that FEF may act as a transitional step in an evolution of coordinates between LIP/MIP and SC. The persistence across cortical areas of mixed representations that do not provide unequivocal location labels in a consistent reference frame has implications for how these representations must be read out. NEW & NOTEWORTHY How we perceive the world as stable using mobile retinas is poorly understood. We compared the stability of visual receptive fields across different fixation positions in three visuomotor regions. Irregular changes in receptive field position were ubiquitous in intraparietal cortex, evident but less common in the frontal eye fields, and negligible in the superior colliculus (SC), where receptive fields shifted reliably across fixations. Only the SC provides a stable labeled-line code for stimuli across saccades.


1995 ◽  
Vol 74 (2) ◽  
pp. 763-769 ◽  
Author(s):  
K. Kishikawa ◽  
H. Uchida ◽  
Y. Yamamori ◽  
J. G. Collins

1. Cats were prepared for chronic recordings from the lumbar enlargement of the spinal dorsal horn. At the beginning of each recording session, a tungsten microelectrode was advanced through the dura in a physiologically intact, awake, drug-free animal, until amplitude discrimination provided a single neuron with a receptive field on the hindquarters. 2. Extracellular recordings of activity of each neuron were made during receptive field stimulation with tactile and thermal nonnoxious and noxious stimuli. 3. Baseline responses obtained in the awake state were compared with responses of the same neurons during slow-wave or rapid-eye-movement (REM) sleep. In a subpopulation of neurons, the effects of anesthesia (propofol, 7.5 mg/kg iv) were observed after the completion of sleep studies. 4. The low-threshold receptive fields of the seven neurons studied during REM sleep were all increased in size when compared with the baseline value. The average increase was 52.6% (range 26.2–96.7%). 5. The low-threshold receptive fields of the seven neurons studied during REM sleep were reduced by propofol anesthesia by an average of 49.1% (range 29–74%). 6. Neuronal response to receptive field brushing was observed in 15 neurons during REM sleep. The effect of propofol on receptive field brushing was observed in 8 of those neurons. In only one of those eight neurons were the effects of REM sleep and anesthesia in the same direction. 7. Changes in neuronal responses were less consistent during slow-wave sleep but still differed from changes induced by propofol.(ABSTRACT TRUNCATED AT 250 WORDS)


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