Development of multisensory processing in ferret parietal cortex.

It is well known that the nervous system adjusts itself to its environment during development. Although a great deal of effort has been directed towards understanding the developmental processes of the individual sensory systems (e.g., vision, hearing, etc.), only one major study has examined the maturation of multisensory processing in cortical neurons. Therefore, the present investigation sought to evaluate multisensory development in a different cortical region and species. Using multiple single-unit recordings in anaesthetised ferrets (n = 18) of different ages (from postnatal day 80 to 300), we studied the responses of neurons from the rostral posterior parietal (PPr) area to presentations of visual, tactile and combined visual-tactile stimulation. The results showed that multisensory neurons were infrequent at the youngest ages (pre-pubertal) and progressively increased through the later ages. Significant response changes that result from multisensory stimulation (defined as multisensory integration [MSI]) were observed in post-pubertal adolescent animals, and the magnitude of these integrated responses also increased across this age group. Furthermore, non-significant multisensory response changes were progressively increased in adolescent animals. Collectively, at the population level, MSI was observed to shift from primarily suppressive levels in infants to increasingly higher levels in later stages. These data indicate that, like the unisensory systems from which it is derived, multisensory processing shows developmental changes whose specific time course may be regionally and species-dependent.

Cortical multisensory connectivity is present near birth in humans.

How the newborn brain adapts to its new multisensory environment has been a subject of debate. Although an early theory proposed that the brain acquires multisensory features as a result of postnatal experience, recent studies have demonstrated that the neonatal brain is already capable of processing multisensory information. For multisensory processing to be functional, it is a prerequisite that multisensory convergence among neural connections occur. However, multisensory connectivity has not been examined in human neonates nor are its location(s) or afferent sources understood. We used resting state functional MRI (fMRI) in two independent cohorts of infants to examine the functional connectivity of two cortical areas known to be multisensory in adults: the intraparietal sulcus (IPS) and the superior temporal sulcus (STS). In the neonate, the IPS was found to demonstrate significant functional connectivity with visual association and somatosensory association areas, while the STS showed significant functional connectivity with the visual association areas, primary auditory cortex, and somatosensory association areas. Our findings establish that each of these areas displays functional communication with cortical regions representing various sensory modalities. This demonstrates the presence of cortical areas with converging sensory inputs, representing that the functional architecture needed for multisensory processing is already present within the first weeks of life.

Overexpression of Serum Response Factor in Neurons Restores Ocular Dominance Plasticity in a Model of Fetal Alcohol Spectrum Disorders.

BACKGROUND: Deficits in neuronal plasticity underlie many neurobehavioral and cognitive problems presented in fetal alcohol spectrum disorder (FASD). Our laboratory has developed a ferret model showing that early alcohol exposure leads to a persistent disruption in ocular dominance plasticity (ODP). For instance, a few days of monocular deprivation results in a robust reduction of visual cortex neurons' responsiveness to stimulation of the deprived eye in normal animals, but not in ferrets with early alcohol exposure. Previously our laboratory demonstrated that overexpression of serum response factor (SRF) exclusively in astrocytes can improve neuronal plasticity in FASD. Here, we test whether neuronal overexpression of SRF can achieve similar effects. METHODS: Ferrets received 3.5 g/kg alcohol intraperitoneally (25% in saline) or saline as control every other day between postnatal day 10 to 30, which is roughly equivalent to the third trimester of human gestation. Animals were given intracortical injections of a Herpes Simplex Virus-based vector to express either green fluorescent protein or a constitutively active form of SRF in infected neurons. They were then monocularly deprived by eyelid suture for 4 to 5 days after which single-unit recordings were conducted to determine whether changes in ocular dominance had occurred. RESULTS: Overexpression of a constitutively active form of SRF by neurons restored ODP in alcohol-treated animals. This effect was observed only in areas near the site of viral infection. CONCLUSIONS: Overexpression of SRF in neurons can restore plasticity in the ferret model of FASD, but only in areas near the site of infection. This contrasts with SRF overexpression in astrocytes which restored plasticity throughout the visual cortex.

Multisensory and unisensory neurons in ferret parietal cortex exhibit distinct functional properties.

Despite the fact that unisensory and multisensory neurons are comingled in every neural structure in which they have been identified, no systematic comparison of their response features has been conducted. Towards that goal, the present study was designed to examine and compare measures of response magnitude, latency, duration and spontaneous activity in unisensory and bimodal neurons from the ferret parietal cortex. Using multichannel single-unit recording, bimodal neurons were observed to demonstrate significantly higher response levels and spontaneous discharge rates than did their unisensory counterparts. These results suggest that, rather than merely reflect different connectional arrangements, unisensory and multisensory neurons are likely to differ at the cellular level. Thus, it can no longer be assumed that the different populations of bimodal and unisensory neurons within a neural region respond similarly to a given external stimulus.

Laminar and connectional organization of a multisensory cortex.

The transformation of sensory signals as they pass through cortical circuits has been revealed almost exclusively through studies of the primary sensory cortices, for which principles of laminar organization, local connectivity, and parallel processing have been elucidated. In contrast, almost nothing is known about the circuitry or laminar features of multisensory processing in higher order, multisensory cortex. Therefore, using the ferret higher order multisensory rostral posterior parietal (PPr) cortex, the present investigation employed a combination of multichannel recording and neuroanatomical techniques to elucidate the laminar basis of multisensory cortical processing. The proportion of multisensory neurons, the share of neurons showing multisensory integration, and the magnitude of multisensory integration were all found to differ by layer in a way that matched the functional or connectional characteristics of the PPr. Specifically, the supragranular layers (L2/3) demonstrated among the highest proportions of multisensory neurons and the highest incidence of multisensory response enhancement, while also receiving the highest levels of extrinsic inputs, exhibiting the highest dendritic spine densities, and providing a major source of local connectivity. In contrast, layer 6 showed the highest proportion of unisensory neurons while receiving the fewest external and local projections and exhibiting the lowest dendritic spine densities. Coupled with a lack of input from principal thalamic nuclei and a minimal layer 4, these observations indicate that this higher level multisensory cortex shows functional and organizational modifications from the well-known patterns identified for primary sensory cortical regions.

An examination of somatosensory area SIII in ferret cortex.

A somatotopically organized region on the suprasylvian gyrus of the ferret was examined using multiunit recordings and anatomical tracer injections. This area, which contains a representation of the face, was bordered by the primary somatosensory area (SI), anteriorly, and by the visually responsive rostral posterior parietal cortex (PPr), posteriorly. Anatomical tracers revealed connections to this region from cortical areas MI, SI, MRSS, PPr, and the thalamic posterior nucleus. These results are consistent with previous work in ferrets as well as with the location, physiology, and connectivity of area SIII in cats. Given its associations, functional properties, location, and homology, it is proposed that this region represents the third cortical somatosensory area (SIII) in ferrets.