Receptive Fields In Superior Colliculus Research Articles

Superior Colliculus: A Vision for Orienting

The superior colliculus contains neurons sensitive to motion direction. New research shows that these neurons are anatomically clustered: those representing the region of visual space 'seen' by both eyes preferentially respond to nasal motion directions and others to opposite directions.

Spatiotemporal structure of visual receptive fields in macaque superior colliculus

Saccades are useful for directing the high-acuity fovea to visual targets that are of behavioral relevance. The selection of visual targets for eye movements involves the superior colliculus (SC), where many neurons respond to visual stimuli. Many of these neurons are also activated before and during saccades of specific directions and amplitudes. Although the role of the SC in controlling eye movements has been thoroughly examined, far less is known about the nature of the visual responses in this area. We have, therefore, recorded from neurons in the intermediate layers of the macaque SC, while using a sparse-noise mapping procedure to obtain a detailed characterization of the spatiotemporal structure of visual receptive fields. We find that SC responses to flashed visual stimuli start roughly 50 ms after the onset of the stimulus and last for on average ~70 ms. About 50% of these neurons are strongly suppressed by visual stimuli flashed at certain locations flanking the excitatory center, and the spatiotemporal pattern of suppression exerts a predictable influence on the timing of saccades. This suppression may, therefore, contribute to the filtering of distractor stimuli during target selection. We also find that saccades affect the processing of visual stimuli by SC neurons in a manner that is quite similar to the saccadic suppression and postsaccadic enhancement that has been observed in the cortex and in perception. However, in contrast to what has been observed in the cortex, decreased visual sensitivity was generally associated with increased firing rates, while increased sensitivity was associated with decreased firing rates. Overall, these results suggest that the processing of visual stimuli by SC receptive fields can influence oculomotor behavior and that oculomotor signals originating in the SC can shape perisaccadic visual perception.

Colour and pattern selectivity of receptive fields in superior colliculus of marmoset monkeys

The main subcortical visual targets of retinal output neurones (ganglion cells) are the parvocellular and magnocellular layers of the dorsal lateral geniculate nucleus (LGN) in the thalamus. In addition, a small and heterogeneous collection of ganglion cell axons projects to the koniocellular layers of the LGN, to the superior colliculus (SC), and to other subcortical targets. The functional (receptive field) properties and target specificity of these non-parvocellular, non-magnocellular populations remain poorly understood. It is known that one population of koniocellular layer cells in the LGN (blue-On cells) receives dominant functional input from short-wavelength sensitive (S or ‘blue') cones. Here we asked whether SC neurones also receive S cone inputs. We made extracellular recordings from single neurones (n = 38) in the SC of anaesthetised marmoset monkeys. Responses to drifting and flashed gratings providing defined levels of cone contrast were measured. The SC receptive fields we recorded were often binocular, showed ‘complex cell' like responses (On–Off responses), strong bandpass spatial frequency tuning, direction selectivity, and many showed strong and rapid habituation to repeatedly presented stimuli. We found no evidence for dominant S cone input to any SC neurone recorded. These data suggest that S cone signals may reach cortical pathways for colour vision exclusively through the koniocellular division of the lateral geniculate nucleus.

Early visual experience prevents but cannot reverse deprivation-induced loss of refinement in adult superior colliculus

The role of sensory experience in the development and plasticity of the visual system has been widely studied. It has generally been reported that once animals reach adulthood, experience-dependent visual plasticity is reduced. We have found that visual experience is not needed for the refinement of receptive fields (RFs) in the superior colliculus (SC) but instead is necessary to maintain them in adulthood (Carrasco et al., 2005). Without light exposure, RFs in SC of hamsters refine by postnatal day 60 as usual but then enlarge, presumably reducing visual acuity. In this study we examine whether a brief period of light exposure during early postnatal development would be sufficient to prevent RF enlargement in adulthood, and whether prolonged light exposure in adulthood could reverse the deprivation-induced increase in RF size. We found that an early postnatal period of at least 30 days of visual experience was sufficient to maintain refined RFs in the adult SC. Prolonged visual experience in adulthood could not reverse the RF enlargement resulting from long-term dark rearing, reflecting a loss of plasticity at this age. Our results suggest that, unlike in visual cortex, dark rearing does not indefinitely extend the critical period of plasticity in SC. Rather, there is a limited time window when early experience can protect RFs from the detrimental effects of visual deprivation in adulthood. These results contribute to understanding adult brain plasticity and argue for the importance of early visual experience in protecting the adult visual system.

Visual Experience Is Necessary for Maintenance But Not Development of Receptive Fields in Superior Colliculus

Sensory deprivation is thought to have an adverse effect on visual development and to prolong the critical period for plasticity. Once the animal reaches adulthood, however, synaptic connectivity is understood to be largely stable. We reported previously that N-methyl-D-aspartate (NMDA) receptor blockade in the superior colliculus of the Syrian hamster prevents refinement of receptive fields (RFs) in normal or compressed retinotopic projections, resulting in target neurons with enlarged RFs but normal stimulus tuning. Here we asked whether visually driven activity is necessary for refinement or maintenance of retinotopic maps or if spontaneous activity is sufficient. Animals were deprived of light either in adulthood only or from birth until the time of recording. We found that dark rearing from birth to 2 mo of age had no effect on the timing and extent of RF refinement as assessed with single unit extracellular recordings. Visual deprivation in adulthood also had no effect. Continuous dark rearing from birth into adulthood, however, resulted in a progressive loss of refinement, resulting in enlarged, asymmetric receptive fields and altered surround suppression in adulthood. Thus unlike in visual cortex, early visually driven activity is not necessary for refinement of receptive fields during development, but is required to maintain refined visual projections in adulthood. Because the map can refine normally in the dark, these results argue against a deprivation-induced delay in critical period closure, and suggest instead that early visual deprivation leaves target neurons more vulnerable to deprivation that continues after refinement.

The influence of visual and auditory receptive field organization on multisensory integration in the superior colliculus.

The spatial register of the different receptive fields of multisensory neurons in the superior colliculus (SC) plays a significant role in determining the responses of these neurons to cross-modal stimulus combinations. Spatially coincident visual-auditory stimuli fall within these overlapping receptive fields and generally produce response enhancements that exceed the individual modality-specific responses and can exceed their sum. Yet, in this context, it has not been clear how "spatial coincidence" is operationally defined. Given the large size of SC receptive fields, visual and auditory stimuli could be within their respective receptive fields even when there are substantial spatial disparities between them. Indeed, previous observations have raised the possibility that there may be a second level of determinism in how SC neurons deal with the relative spatial locations of within-field cross-modal stimuli; specifically, that multisensory response enhancements become progressively weaker as the within-field visual and auditory stimuli become increasingly disparate. While the present experiments demonstrated that SC multisensory neurons have heterogeneous receptive fields, and that the greatest number of impulses evoked were by stimuli that fell within the area of cross-modal receptive field overlap, they also indicate that there is no systematic relationship between cross-modal stimulus disparity and the magnitude of multisensory response enhancement. Thus, two within-field cross-modal stimuli produced the same proportionate change (i.e., multisensory response enhancement) when they were widely disparate as they did when they overlapped one another in space. These observations indicate that cross-modal spatial coincidence can be defined operationally by the borders of an SC neuron's receptive fields regardless of the size of those receptive fields and/or the absolute spatial disparity between within-field cross-modal stimuli.

The contribution of protein kinases to plastic events in the superior colliculus

1. l The superior colliculus (SC) / optic tectum is a multi-layered midbrain area that harbours representations of visual and auditory space and somatic body surface. The development and maintenance of these sensory maps has been shown to involve activity and experience-dependent mechanisms. 2. 2. The implantation of an extra eye primordium into the developing forebrain ofRana pipens results in the formation of dually innervated tecta that would have normally be solely innervated by the contralateral retina. The retinal projections are arranged in an interdigitating pattern of alternate stripes of terminations from each retina. The establishment of this striped pattern requires retinal activity and depends on N-methyl-D-aspartate (NMDA) receptors. Manipulation of protein kinase activity leads to the formation of an abnormal stripe pattern. 3. 3 Regeneration of the goldfish retinotectal projection, following crush of the optic nerve, occurs in an activity dependent manner involving NMDA receptors. Furthermore, a critical period exists, during which retinal activity is vital for reformation of the visual map. Protein kinase manipulations during this period disrupt normal reformation. The same manoeuvres at other time points have little effect on map reformation. 4. 4 An unusual form of long-term potentiation (SC-LTP) has been demonstrated in the in vitro preparation of the guinea-pig SC. By stimulating the optic layer of the SC, a postsynaptic potentiation can be recorded in the superficial grey layer. The expression of SC-LTP is masked but not prevented by blockade of NMDA receptors. The role of protein kinases in this form of synaptic modification has also been studied using various manipulations and inhibitors with varying substrate specificity. Whereas H7, an inhibitor reputed to be protein kinase C specific, only masks the expression of SC-LTP, K252a which has a broad substrate specificity blocks the induction of SC-LTP. 5. 5 Experience-dependent formation of the auditory space map in the deeper layers of the SC is believed to be under the instruction of the visual representation in the superficial layers. Furthermore, a crucial period exists during which normal auditory and visual experience are required for successful establishment of the auditory map. Chronic exposure to 5-aminophosphonopentanoic acid (AP5) during this time prevents the formation of the map. Chronic exposure to K252a, a broad kinase inhibitor, over the same time period, also disrupts the formation of the auditory space map. 6. 6. Taken together, these models emphasise the role of protein kinases in synaptic plasticity observed in the SC. Furthermore, interference with protein kinase activity at crucial stages of regeneration or development appears to disrupt the sequence of events that lead to the consolidation of SC receptive fields.

Importance of corpus callosum for visual receptive fields of single neurons in cat superior colliculus

1. Section of the posterior two-thirds of the corpus callosum eliminates almost completely the response of superior colliculus (SC) neurons to stimulation of the contralateral eye in split-chiasm cats. On the contrary, the responsiveness of SC neurons to stimulation of the contralateral eye is not abolished by a transection of the posterior and tectal commissures leaving the corpus callosum intact. The callosal section also reduces the number of SC receptive fields abutting the vertical meridian in the ipsilateral eye of split-chiasm cats. 2. In cats with intact optic pathways, a similar callosal section abolishes the SC representation of the ipsilateral visual field in the ipsilateral eye and also reduces the number of receptive fields adjoining the vertical meridian in the same eye. In the contralateral eye, the SC representation of the ipsilateral visual field is reduced in extension to about one-fifth of that seen in cats with intact commissures. 3. The results suggest that the corpus callosum is the main pathway for cross-midline communication of visual information at not only the cortical, but also the midbrain level. The corpus callosum may subserve this function because it contains uninterrupted crossed corticotectal projections or because it transmits visual information from one hemisphere to contralateral cortical areas projecting ipsilaterally to SC. The latter hypothesis is more likely but, in any case, the findings imply that the lack of interhemispheric transfer of visual learning in cats with a chiasmatic and callosal section may depend on a midline disconnection of both subcortical and cortical visual centers. 4. The corpus callosum is also responsible for the representation of the ipsilateral visual field of the ipsilateral eye in the cat SC. The SC representation of the ipsilateral visual field in the contralateral eye is due, in minimal part, to direct retinotectal connections from temporal retina and, for the largest part, to the corpus callosum. 5. Finally, the corpus callosum contributes to the representation of the contralateral visual field near the vertical meridian of the temporal retina in both split-chiasm and normal cats. This is probably due to the scarcity of direct retinotectal projections from this part of the retina and to their supplementation by corticotectal neurons influenced by the callosal afferents.

Effects of monocular lid closure on development of receptive-field characteristics of neurons in rabbit superior colliculus.

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.

Indirect, across-the-midline retinotectal projections and representation of ipsilateral visual field in superior colliculus of the cat.

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...

Effects of extraocular muscle section on receptive fields in cat superior colliculus

In order to find out whether changes in the ocular dominance histograms of the visual cortex are mirrored in the superior colliculus, we sectioned cats' right medial and right lateral reclus muscles during the second week of life. We found that most cells in the superior colliculus contralateral to the unoperated eye become dominated by the unoperated eye, while most cells in the superior colliculus contralateral to the operated eye remain binocularly driven. In contrast, most cells in each visual cortex become monocularly driven, some by the operated eye, others by the unoperated eye. Squint surgery does not change the proportion of directionally selective cells in the superior colliculus, but does change the distribution of preferred directions, increasing the proportion of cells preferring approximately vertical simulus movement. These results suggest that the ability to move the eyes normally is important for the maintenance of normal receptive fields in the superior colliculus.