Diana K. Sarko

Identifying and Quantifying Multisensory Integration: A Tutorial Review

We process information from the world through multiple senses, and the brain must decide what information belongs together and what information should be segregated. One challenge in studying such multisensory integration is how to quantify the multisensory interactions, a challenge that is amplified by the host of methods that are now used to measure neural, behavioral, and perceptual responses. Many of the measures that have been developed to quantify multisensory integration (and which have been derived from single unit analyses), have been applied to these different measures without much consideration for the nature of the process being studied. Here, we provide a review focused on the means with which experimenters quantify multisensory processes and integration across a range of commonly used experimental methodologies. We emphasize the most commonly employed measures, including single- and multiunit responses, local field potentials, functional magnetic resonance imaging, and electroencephalography, along with behavioral measures of detection, accuracy, and response times. In each section, we will discuss the different metrics commonly used to quantify multisensory interactions, including the rationale for their use, their advantages, and the drawbacks and caveats associated with them. Also discussed are possible alternatives to the most commonly used metrics.

Cellular scaling rules of insectivore brains

Insectivores represent extremes in mammalian body size and brain size, retaining various “primitive” morphological characteristics, and some species of Insectivora are thought to share similarities with small-bodied ancestral eutherians. This raises the possibility that insectivore brains differ from other taxa, including rodents and primates, in cellular scaling properties. Here we examine the cellular scaling rules for insectivore brains and demonstrate that insectivore scaling rules overlap somewhat with those for rodents and primates such that the insectivore cortex shares scaling rules with rodents (increasing faster in size than in numbers of neurons), but the insectivore cerebellum shares scaling rules with primates (increasing isometrically). Brain structures pooled as “remaining areas” appear to scale similarly across all three mammalian orders with respect to numbers of neurons, and the numbers of non-neurons appear to scale similarly across all brain structures for all three orders. Therefore, common scaling rules exist, to different extents, between insectivore, rodent, and primate brain regions, and it is hypothesized that insectivores represent the common aspects of each order. The olfactory bulbs of insectivores, however, offer a noteworthy exception in that neuronal density increases linearly with increasing structure mass. This implies that the average neuronal cell size decreases with increasing olfactory bulb mass in order to accommodate greater neuronal density, and represents the first documentation of a brain structure gaining neurons at a greater rate than mass. This might allow insectivore brains to concentrate more neurons within the olfactory bulbs without a prohibitively large and metabolically costly increase in structure mass.

Adaptations in the structure and innervation of follicle-sinus complexes to an aquatic environment as seen in the Florida manatee (Trichechus manatus latirostris)

Florida manatees are large‐bodied aquatic herbivores that use large tactile vibrissae for several purposes. Facial vibrissae are used to forage in a turbid water environment, and the largest perioral vibrissae can also grasp and manipulate objects. Other vibrissae distributed over the entire postfacial body appear to function as a lateral line system. All manatee vibrissae emanate from densely innervated follicle‐sinus complexes (FSCs) like those in other mammals, although proportionately larger commensurate with the caliber of the vibrissae. As revealed by immunofluorescence, all manatee FSCs have many types of C, Aδ and Aβ innervation including Merkel, club, and longitudinal lanceolate endings at the level of the ring sinus, but they lack other types such as reticular and spiny endings at the level of the cavernous sinus. As in non‐whisking terrestrial species, the inner conical bodies of facial FSCs are well innervated but lack Aβ‐fiber terminals. Importantly, manatee FSCs have two unique types of Aβ‐fiber endings. First, all of the FSCs have exceptionally large‐caliber axons that branch to terminate as novel, gigantic spindle‐like endings located at the upper ring sinus. Second, facial FSCs have smaller caliber Aβ fibers that terminate in the trabeculae of the cavernous sinus as an ending that resembles a Golgi tendon organ. In addition, the largest perioral vibrissae, which are used for grasping, have exceptionally well‐developed medullary cores that have a structure and dense small‐fiber innervation resembling that of tooth pulp. Other features of the epidermis and upper dermis structure and innervation differ from that seen in terrestrial mammals. J. Comp. Neurol. 504:217–237, 2007.

Mammalian tactile hair: divergence from a limited distribution

Mammalian species use tactile hairs to address a variety of perceptual challenges in detecting and responding appropriately to environmental stimuli. With a wide range of functional roles that range from object detection, to fine texture discrimination, to hydrodynamic trail perception, tactile hairs have been adapted for a variety of environmental niches to enhance survival through optimizing detection of somatosensory cues. Because the high level of innervation associated with tactile hairs requires a commensurately high dedication of neural resources, their distribution is restricted to specific regions of the body that encounter stimuli of interest—commonly, the face. However, several species—namely bats, naked mole‐rats, hyraxes, manatees, and dugongs—are rare exceptions, with tactile hair distribution that has expanded to cover the entire body. This review examines the behavioral advantages conferred by this unusual trait, the neuroanatomical adaptations that accompany it, and how this pattern might have evolved.

Somatosensory Areas of Manatee Cerebral Cortex: Histochemical Characterization and Functional Implications

A histochemical and cytoarchitectural analysis was completed for the neocortex of the Florida manatee in order to localize primary sensory areas and particularly primary somatosensory cortex (SI). Based on the location of cytochrome oxidase-dense staining in flattened cortex preparations, preliminary functional divisions were assigned for SI with the face represented laterally followed by the flipper, body and tail representations proceeding medially. The neonate exhibited four distinct patches in the frontoparietal cortex (presumptive SI), whereas juvenile and adult specimens demonstrated a distinct pattern in which cytochrome oxidase-dense staining appeared to be blended into one large patch extending dorsomedially. This differential staining between younger versus older more developed animals was also seen on coronal sections stained for cytochrome oxidase, myelin, or Nissl bodies. These were systematically analyzed in order to accurately localize the laminar and cytoarchitectural extent of cytochrome oxidase staining. Overall, SI appears to span seven cytoarchitectural areas to which we have assigned presumptive functional representations based on the relative locations of cytochrome oxidase-dense staining.

Convergent approaches toward the study of multisensory perception.

Classical analytical approaches for examining multisensory processing in individual neurons have relied heavily on changes in mean firing rate to assess the presence and magnitude of multisensory interaction. However, neurophysiological studies within individual sensory systems have illustrated that important sensory and perceptual information is encoded in forms that go beyond these traditional spike-based measures. Here we review analytical tools as they are used within individual sensory systems (auditory, somatosensory, and visual) to advance our understanding of how sensory cues are effectively integrated across modalities (e.g., audiovisual cues facilitating speech processing). Specifically, we discuss how methods used to assess response variability (Fano factor, or FF), local field potentials (LFPs), current source density (CSD), oscillatory coherence, spike synchrony, and receiver operating characteristics (ROC) represent particularly promising tools for understanding the neural encoding of multisensory stimulus features. The utility of each approach and how it might optimally be applied toward understanding multisensory processing is placed within the context of exciting new data that is just beginning to be generated. Finally, we address how underlying encoding mechanisms might shape—and be tested alongside with—the known behavioral and perceptual benefits that accompany multisensory processing.

Compartmentation of the Cerebellar Cortex in the Naked Mole-Rat (Heterocephalus glaber)

Despite the apparent uniformity in cellular composition of the adult mammalian cerebellar cortex, it is actually highly compartmentalized into transverse zones and within each zone further subdivided into a reproducible array of parasagittal stripes. This basic cerebellar architecture is highly conserved in birds and mammals. However, different species have very different cerebellar morphologies, and it is unclear if cerebellar architecture reflects taxonomic relations or ecological niches. To explore this, we have examined the cerebellum of the naked mole-rat Heterocephalus glaber, a burrowing rodent with adaptations to a subterranean life that include only a rudimentary visual system. The cerebellum of H. glaber resembles that of other rodents with the remarkable exception that cerebellar regions that are prominent in the handling of visual information (the central zone, nodular zone, and dorsal paraflocculus) are greatly reduced or absent. In addition, there is a notable increase in size in the posterior zone, consistent with an expanded role for the trigeminal somatosensory system. These data suggest that cerebellar architecture may be substantially modified to serve a particular ecological niche.

Manatee vibrissae: evidence for a “lateral line” function

Aquatic mammals use vibrissae to detect hydrodynamic stimuli over a range from 5 to 150 Hz, similar to the range detected by lateral line systems in fishes and amphibians. Manatees possess ∼5,300 vibrissae distributed over the body, innervated by ∼209,000 axons. This extensive innervation devoted to vibrissae follicles is reflected in enlarged, elaborate somatosensory regions of the gracile, cuneate, and Bischoffs brain‐stem nuclei, ventrobasal thalamus, and presumptive somatosensory cortex. Our preliminary psychophysical testing indicates that in Florida and Antillean manatees the Weber fraction for detection thresholds for grating textures ranges from 0.025 to 0.14. At the lower end of this range, sensitivity is comparable to human index finger thresholds. For hydrodynamic stimuli of 5–150 Hz, detection threshold levels for manatees using facial or postfacial vibrissae were substantially lower than those reported for harbor seals and similar to reports of sensitivity for the lateral line systems of some fish. Our findings suggest that the facial and postfacial vibrissae are used to detect hydrodynamic stimuli, whereas only the facial vibrissae are used for direct contact investigation.

Somatosensory Nuclei of the Manatee Brainstem and Thalamus

Florida manatees have an extensive, well‐developed system of vibrissae distributed over their entire bodies and especially concentrated on the face. Although behavioral and anatomical assessments support the manatees reliance on somatosensation, a systematic analysis of the manatee thalamus and brainstem areas dedicated to tactile input has never been completed. Using histochemical and histological techniques (including stains for myelin, Nissl, cytochrome oxidase, and acetylcholinesterase), we characterized the relative size, extent, and specializations of somatosensory regions of the brainstem and thalamus. The principal somatosensory regions of the brainstem (trigeminal, cuneate, gracile, and Bischoffs nucleus) and the thalamus (ventroposterior nucleus) were disproportionately large relative to nuclei dedicated to other sensory modalities, providing neuroanatomical evidence that supports the manatees reliance on somatosensation. In fact, areas of the thalamus related to somatosensation (the ventroposterior and posterior nuclei) and audition (the medial geniculate nucleus) appeared to displace the lateral geniculate nucleus dedicated to the subordinate visual modality. Furthermore, it is noteworthy that, although the manatee cortex contains Rindenkerne (barrel‐like cortical nuclei located in layer VI), no corresponding cell clusters were located in the brainstem (“barrelettes”) or thalamus (“barreloids”). Anat Rec, 290:1138–1165, 2007.

Organization of somatosensory cortex in the northern grasshopper mouse (Onychomys leucogaster), a predatory rodent

Northern grasshopper mice (Onychomys leucogaster) are among the most highly carnivorous rodents in North America. Because predatory mammals may have specialization of senses used to detect prey, we investigated the organization of sensory areas within grasshopper mouse neocortex and quantified the number of myelinated axons in grasshopper mouse trigeminal, cochlear, and optic nerves. Multiunit electrophysiological recordings combined with analysis of flattened sections of neocortex processed for cytochrome oxidase were used to determine the topography of primary somatosensory cortex (S1) and the location and size of both the visual and auditory cortex in adult animals. These findings were then related to the distinctive chemoarchitecture of layer IV visible in flattened cortical sections of juvenile grasshopper mice labeled with the serotonin transporter (SERT) antibody, revealing a striking correspondence between electrophysiological maps and cortical anatomy. J. Comp. Neurol. 519:64‐74, 2011.