Somatosensory substrates of flight control in bats.

Flight maneuvers require rapid sensory integration to generate adaptive motor output. Bats achieve remarkable agility with modified forelimbs that serve as airfoils while retaining capacity for object manipulation. Wing sensory inputs provide behaviorally relevant information to guide flight; however, components of wing sensory-motor circuits have not been analyzed. Here, we elucidate the organization of wing innervation in an insectivore, the big brown bat, Eptesicus fuscus. We demonstrate that wing sensory innervation differs from other vertebrate forelimbs, revealing a peripheral basis for the atypical topographic organization reported for bat somatosensory nuclei. Furthermore, the wing is innervated by an unusual complement of sensory neurons poised to report airflow and touch. Finally, we report that cortical neurons encode tactile and airflow inputs with sparse activity patterns. Together, our findings identify neural substrates of somatosensation in the bat wing and imply that evolutionary pressures giving rise to mammalian flight led to unusual sensorimotor projections.

Neural latencies across auditory cortex of macaque support a dorsal stream supramodal timing advantage in primates.

Sensory systems across the brain are specialized for their input, yet some principles of neural organization are conserved across modalities. The pattern of anatomical connections from the primate auditory cortex to the temporal, parietal, and prefrontal lobes suggests a possible division into dorsal and ventral auditory processing streams, with the dorsal stream originating from more caudal areas of the auditory cortex, and the ventral stream originating from more rostral areas. These streams are hypothesized to be analogous to the well-established dorsal and ventral streams of visual processing. In the visual system, the dorsal processing stream shows substantially faster neural response latencies than does the ventral stream. However, the relative timing of putative dorsal and ventral stream processing has yet to be explored in other sensory modalities. Here, we compare distributions of neural response latencies from 10 different areas of macaque auditory cortex, confirmed by individual anatomical reconstructions, to determine whether a similar timing advantage is found for the hypothesized dorsal auditory stream. Across three varieties of auditory stimuli (clicks, noise, and pure tones), we find that latencies increase with hierarchical level, as predicted by anatomical connectivity. Critically, we also find a pronounced timing differential along the caudal-to-rostral axis within the same hierarchical level, with caudal (dorsal stream) latencies being faster than rostral (ventral stream) latencies. This observed timing differential mirrors that found for the dorsal stream of the visual system, suggestive of a common timing advantage for the dorsal stream across sensory modalities.

Auditory cortical tuning to band-pass noise in primate A1 and CM: a comparison to pure tones.

We examined multiunit responses to tones and to 1/3 and 2/3 octave band-pass noise (BPN) in the marmoset primary auditory cortex (A1) and the caudomedial belt (CM). In both areas, BPN was more effective than tones, evoking multiunit responses at lower intensity and across a wider frequency range. Typically, the best responses to BPN remained at the characteristic frequency. Additionally, in both areas responses to BPN tended to be of greater magnitude and shorter latency than responses to tones. These effects are consistent with the integration of more excitatory inputs driven by BPN than by tones. While it is generally thought that single units in A1 prefer narrow band sounds such as tones, we found that best responses for multi units in both A1 and CM were obtained with noises of narrow spectral bandwidths.

Coding of FM sweep trains and twitter calls in area CM of marmoset auditory cortex.

The primate auditory cortex contains three interconnected regions (core, belt, parabelt), which are further subdivided into discrete areas. The caudomedial area (CM) is one of about seven areas in the belt region that has been the subject of recent anatomical and physiological studies conducted to define the functional organization of auditory cortex. The main goal of the present study was to examine temporal coding in area CM of marmoset monkeys using two related classes of acoustic stimuli: (1) marmoset twitter calls; and (2) frequency-modulated (FM) sweep trains modeled after the twitter call. The FM sweep trains were presented at repetition rates between 1 and 24 Hz, overlapping the natural phrase frequency of the twitter call (6-8 Hz). Multiunit recordings in CM revealed robust phase-locked responses to twitter calls and FM sweep trains. For the latter, phase-locking quantified by vector strength (VS) was best at repetition rates between 2 and 8 Hz, with a mean of about 5 Hz. Temporal response patterns were not strictly phase-locked, but exhibited dynamic features that varied with the repetition rate. To examine these properties, classification of the repetition rate from the temporal response pattern evoked by twitter calls and FM sweep trains was examined by Fisher's linear discrimination analysis (LDA). Response classification by LDA revealed that information was encoded not only by phase-locking, but also other components of the temporal response pattern. For FM sweep trains, classification was best for repetition rates from 2 to 8 Hz. Thus, the majority of neurons in CM can accurately encode the envelopes of temporally complex stimuli over the behaviorally-relevant range of the twitter call. This suggests that CM could be engaged in processing that requires relatively precise temporal envelope discrimination, and supports the hypothesis that CM is positioned at an early stage of processing in the auditory cortex of primates.

Multisensory space representations in the macaque ventral intraparietal area.

Animals can use different sensory signals to localize objects in the environment. Depending on the situation, the brain either integrates information from multiple sensory sources or it chooses the modality conveying the most reliable information to direct behavior. This suggests that somehow, the brain has access to a modality-invariant representation of external space. Accordingly, neural structures encoding signals from more than one sensory modality are best suited for spatial information processing. In primates, the posterior parietal cortex (PPC) is a key structure for spatial representations. One substructure within human and macaque PPC is the ventral intraparietal area (VIP), known to represent visual, vestibular, and tactile signals. In the present study, we show for the first time that macaque area VIP neurons also respond to auditory stimulation. Interestingly, the strength of the responses to the acoustic stimuli greatly depended on the spatial location of the stimuli [i.e., most of the auditory responsive neurons had surprisingly small spatially restricted auditory receptive fields (RFs)]. Given this finding, we compared the auditory RF locations with the respective visual RF locations of individual area VIP neurons. In the vast majority of neurons, the auditory and visual RFs largely overlapped. Additionally, neurons with well aligned visual and auditory receptive fields tended to encode multisensory space in a common reference frame. This suggests that area VIP constitutes a part of a neuronal circuit involved in the computation of a modality-invariant representation of external space.

Neurosurgical access to cortical areas in the lateral fissure of primates.

In this report, a method is presented for gaining direct access to cortical areas within the lateral fissure of primates for neuroanatomical tracer injections and electrode array implantation. Compared to areas on the surface of the brain, the anatomical and physiological properties of areas within the fissure are poorly understood. Typically, access to these areas is indirectly achieved by ablating or passing through intervening areas. To enable direct experimental access, a neurosurgical technique was developed in primates whereby the banks of the lateral fissure were retracted with sparing of the vascular network and intervening areas. In some animals, anatomical tracers were directly injected into target fields without contamination of other areas. In others, multichannel electrode arrays were implanted into target areas for chronic recording of neural activity. Since, these techniques could be adapted for exploration of areas within other sulci, the approach represents an important advance in efforts to elucidate the functional organization of the primate cerebral cortex.

GABA( A) synapses shape neuronal responses to sound intensity in the inferior colliculus.

Neurons in the inferior colliculus (IC) change their firing rates with sound pressure level. Some neurons maintain monotonic increases in firing rate over a wide range of sound intensities, whereas other neurons are monotonic over limited intensity ranges. We examined the conditions necessary for monotonicity in this nucleus in vitro in rat brain slices and in vivo in the unanesthetized rabbit. Our in vitro recordings indicate that concurrent activation of GABA(A) synapses with excitatory inputs facilitates monotonic increases in firing rate with increases in stimulus strength. In the absence of synaptic inhibition, excitatory input to IC neurons causes large depolarizations that result in firing block and nonmonotonicity. In vivo, although GABA(A) synapses decrease the firing rate in all IC neurons, they can have opposing effects on rate-level functions. GABAergic inputs activated by all sound intensities maintain monotonicity by keeping the postsynaptic potential below the level at which depolarization block occurs. When these inputs are blocked, firing block can occur and rate-level functions become nonmonotonic. High-threshold GABAergic inputs, in contrast, cause nonmonotonic responses by decreasing the firing rate at high intensities. Our results suggest that a dynamic regulation of the postsynaptic membrane potential by synaptic inhibition is necessary to allow neurons to respond monotonically to a wide range of sound intensities.