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. 2001 Nov 15;21(22):8886-94.
doi: 10.1523/JNEUROSCI.21-22-08886.2001.

Sensory and multisensory responses in the newborn monkey superior colliculus

Affiliations

Sensory and multisensory responses in the newborn monkey superior colliculus

M T Wallace et al. J Neurosci. .

Abstract

Superior colliculus (SC) neurons have the ability to synthesize information from different sensory modalities, resulting in enhancements (or depressions) of their activity. This physiological capacity is, in turn, closely tied to changes in overt attentive and orientation responses. The present study shows that, in contrast to more altricial species, many deep layer SC neurons in the rhesus monkey are multisensory at birth. Such neurons can respond to stimuli from different sensory modalities, and all convergence patterns seen in the adult are represented. Nevertheless, these neurons cannot yet synthesize their multisensory inputs. Rather, they respond to combinations of cross-modal stimuli much like they respond to their individual modality-specific components. This immature property of multisensory neurons is in contrast to many of the surprisingly sophisticated modality-specific response properties of these neurons and of their modality-specific neighbors. Thus, although deep SC neurons in the newborn have longer latencies and larger receptive fields than their adult counterparts, they are already highly active and are distributed in the typical adult admixture of visual, auditory, somatosensory, and multisensory neurons. Furthermore, the receptive fields of these neurons are already ordered into well organized topographic maps, and the different receptive fields of the same multisensory neurons show a good degree of cross-modal spatial register. These data, coupled with those from cat, suggest that the capacity to synthesize multisensory information does not simply appear in SC neurons at a prescribed maturational stage but rather develops only after substantial experience with cross-modal cues.

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Figures

Fig. 1.
Fig. 1.
Visual, auditory, and somatosensory latencies are significantly longer in the SC of the newborn (black) than in the SC of the adult (gray). Thearrow in each distribution represents the population mean.
Fig. 2.
Fig. 2.
Modality convergence patterns in the SC of the newborn and adult (inset) monkey. Pie charts show the distributions of all recorded sensory-responsive neurons in the multisensory laminas (IV–VII) of the SC.
Fig. 3.
Fig. 3.
The receptive fields of SC neurons are larger in neonates than in adults. Representative receptive fields (shading) of multisensory and modality-specific neurons, at comparable sites in the multisensory laminas of the newborn (left) and adult (right) SC, are shown on schematics of visual and auditory space and on drawings of the body surface. In the schematics of visual and auditory space,straight lines illustrate the horizontal and vertical meridians, and each concentric circle represents 10°. The half-circle in the auditory schematic represents the caudal half of auditory space. For illustrative purposes, all receptive fields are shown in right (contralateral) sensory space. In thecenter are plotted the relationships between size and location of modality-specific and multisensory receptive fields. Visual and auditory receptive fields are plotted in areal extent. Somatosensory receptive fields are normalized to represent a percentage of the total body surface, and the somatosensory graph contains only receptive fields whose centers are located on the front half of the body (see Results). Note that, regardless of the modality, modality convergence pattern, or the locations of the receptive field centers of a neuron, neonatal receptive fields (dark symbols and solid lines) are larger than those of their adult counterparts (lighter symbols anddashed lines). S, Superior;I, inferior; N, nasal; T, temporal.
Fig. 4.
Fig. 4.
Receptive fields in the newborn's SC shifted systematically as neurons were sampled at progressively more caudal locations. The middle schematic illustrates the path of an electrode on a drawing of a parasagittal section. Each of the symbols represents a sensory-responsive neuron whose receptive field(s) was mapped. Note that, as the electrode advanced, the progression of receptive fields (shading) was from those representing frontal or rostral sensory space to those representing temporal or caudal sensory space. Boxeshighlight the receptive fields of multisensory neurons.Numbers represent the recorded depth of each neuron from the surface of the SC. Conventions are the same as in Figure 3.Sup, Superficial layers; Deep, multisensory layers; PAG, periaqueductal gray;IC, inferior colliculus.
Fig. 5.
Fig. 5.
Neurons in the SC of the newborn monkey failed to exhibit mature multisensory integration. Top panels illustrate the auditory and somatosensory receptive fields (shading) of a multisensory neuron in the newborn, as well as the locations of test stimuli (speaker icon and somatosensory probe). Rasters, peristimulus time histograms, summary bar graphs, and oscillographic traces show the responses of this neuron to an auditory stimulus (left), to a somatosensory stimulus (middle), and to their multisensory combination (right). The duration of the auditory (A; square wave shows white-noise burst) and somatosensory (S; ramp shows probe movement) stimuli are shown. Oscillographic traces at the bottom show the responses of this neuron to a single presentation of each stimulus. Note that the responses to the cross-modal stimulus combination differ little from the responses to the more effective of the two modality-specific stimuli.
Fig. 6.
Fig. 6.
The newborn's multisensory responses were no different from its modality-specific responses. Multisensory SC responses are plotted here as a proportion of the dominant modality-specific response (newborn, left; adult,right). Note that the newborn's multisensory responses differ little from its dominant modality-specific responses (left), whereas these responses differ substantially in the adult (right). *p < 0.01.
Fig. 7.
Fig. 7.
Multisensory response enhancements were not evoked in the newborn's SC, regardless of the spatial or temporal relationship of the cross-modal stimuli or their level of effectiveness. A, The visual (darker shading) and auditory (lighter shading) receptive fields of representative multisensory neurons from the newborn and adult are shown in the middle. In these examples, a stationary within-field auditory stimulus (A) was paired with a moving visual stimulus at three different locations within the visual receptive field (V1,V2, and V3). Summary bar graphs show that, in the newborn, these three cross-modal stimulus pairings (V1A, V2A, and V3A) produced responses that approximated those evoked by the dominant modality-specific stimulus, but in the adult, similar pairings produced substantial multisensory response enhancements.B, Multisensory response enhancements peaked at certain cross-modal SOAs in the adult (gray symbols and dashed line), but varying SOA had little impact on the responses of multisensory neurons in the newborn (black symbols and solid line).C, Similarly, multisensory response enhancement in the adult often peaked at low levels of stimulus effectiveness (gray symbols and dashed line), but manipulations of this stimulus parameter had little impact on the multisensory product in neonatal SC neurons (black symbols and solid line). *p< 0.05.

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