Development of Multisensory Neurons and Multisensory Integration in Cat Superior Colliculus

By Mark T. Wallace, Barry E. Stein. 1997

The development of multisensory neurons and multisensory integration was examined in the deep layers of the superior colliculus of kittens ranging in age from 3 to 135 d postnatal (dpn). Despite the high proportion of multisensory neurons in adult animals, no such neurons were found during the first 10 d of postnatal life. Rather, all sensory-responsive neurons were unimodal. The first multisensory neurons (somatosensory–auditory) were found at 12 dpn, and visually responsive multisensory neurons were not found until 20 dpn. Early multisensory neurons responded weakly to sensory stimuli, had long latencies, large receptive fields, and poorly developed response selectivities. Most surprising, however, was their inability to integrate combinations of sensory cues to produce significant response enhancement (or depression), a characteristic feature of the adult. Responses to combinations of sensory cues differed little from responses to their modality-specific components. At 28 dpn an abrupt physiological change was noted. Some multisensory neurons now integrated combinations of cross-modality cues and exhibited significant response enhancements when these cues were spatially coincident and response depressions when the cues were spatially disparate. During the next 2 months the incidence of multisensory neurons, and the proportion of these neurons capable of adult-like multisensory integration, gradually increased. Once multisensory integration appeared in a given neuron, its properties changed little with development. Even the youngest integrating neurons showed superadditive enhancements and spatial characteristics of multisensory integration that were indistinguishable from the adult. Nevertheless, neonatal and adult multisensory neurons differed in the manner in which they integrated temporally asynchronous stimuli, a distribution that may reflect the very different behavioral requirements at different ages. The possible maturational role of corticotectal projections in the abrupt gating of multisensory integration is discussed.

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Citations in the corpus

Early Experience & Multisensory Perceptual Narrowing (2014, background): “…only begin emerging after birth, that they do not integrate multisensory signals when they emerge, and that their ability to integrate auditory, visual, and tactile localization cues depends on the specific spatial alignment of these cues early in life (Wallace & Stein, 1997, 2000, 2001, 2007).”
Development and Plasticity of Intra- and Intersensory Information Processing (2008, background): “…the adult tonotopic map specific to stimuli that predict behaviorally reinforcing events, the degree to which the cue frequency is overrepresented in the tonotopic map is positively correlated with the animal’s learned proficiency in the frequency discrimination task (Polley et al, 2006).”
Onset of cross-modal synthesis in the neonatal superior colliculus is gated by the development of cortical influences. (2000, methodology): “M E T H O D S Procedures were conducted in accordance with the guidelines established by the Institutional Animal Care and Use Committee of Wake Forest University, are identical to those previously reported (Wallace and Stein 1994, 1997), and will be described only briefly.”
Selective Attention and Multisensory Integration: Multiple Phases of Effects on the Evoked Brain Activity (2005, background): “For instance , single-cell recordings in animals have shown that there are polymodal representations of external space in the superior colliculus of cats (e.g., Wallace, Meredith, & Stein, 1998; Wallace & Stein, 1997) and monkeys (Wallace & Stein, 2001).”
The development of intersensory temporal perception: an epigenetic systems/limitations view. (2000, background): “Wallace and Stein's (1997) findings indicate that the neural substrate for intersensory spatial integration is immature and not fully developed in early infancy.”
The Construct of the Multisensory Temporal Binding Window and its Dysregulation in Developmental Disabilities (2014, background): “Animal model studies have shown that multisensory neurons and their associated integrative properties mature over a protracted period of developmental life that extends well into “adolescence” (Wallace & Stein, 1997; Wallace, McHaffie, & Stein, 1997; Wallace, 2004a, 2004b; Wallace et al., 2006).”
Perceptual training narrows the temporal window of multisensory binding (2009, background): “…highlighted that significant changes take place in multisensory temporal processing as maturation progresses (Lewkowicz, 1996; Wallace et al., 1997; Wallace and Stein, 1997; Lewkowicz and Ghazanfar, 2006; Lewkowicz et al., 2008), few studies have looked at the possible malleability of these…”
Development of multisensory spatial integration and perception in humans. (2006, background): “Several developmental studies in both cats and monkeys suggest that these multisensory neurons, abundant in the adult, are either lacking or incapable of this integrative function in newborns (Wallace & Stein, 1997, 2001).”
Incorporating Cross-Modal Statistics in the Development and Maintenance of Multisensory Integration (2012, background): “Its maturation has been examined most closely in the cat, an altricial species whose neonatal SC neurons are unisensory (Stein et al., 1973) but gradually acquire multisensory response properties over many postnatal weeks (Wallace and Stein, 1997).”
Early experience determines how the senses will interact. (2007, methodology): “However, despite its utility it does not appear to be an innate ability because the earliestappearing multisensory neurons in the superior colliculus (SC) are incapable of synthesizing cross-modal stimuli (Stein et al. 1973; Wallace and Stein 1997, 2001).”