Thalamic nuclei are thought to funnel sensory information to the brain's primary cortical areas, which in turn transmit signals afresh to higher cortical areas. Here we describe a direct projection in the macaque monkey from the lateral geniculate nucleus (LGN) to the motion-selective middle temporal area (MTor V5), a cortical area not previously considered 'primary'. The constituent neurons are mostly koniocellular, send virtually no collateral axons to primary visual cortex (V1) and equal about 10% of the V1 population innervating MT. This pathway could explain the persistence of motion sensitivity in subjects following injury to V1, suggesting more generally that residual perception after damage in a primary area may arise from sparse thalamic input to 'secondary' cortical areas.
Birdsong is a learned behavior remarkable for its high degree of stereotypy. Nevertheless, adult birds display substantial rendition-byrendition variation in the structure of individual song elements or "syllables." Previous work suggests that some of this variation is actively generated by the avian basal ganglia circuitry for purposes of motor exploration. However, it is unknown whether and how natural variations in premotor activity drive variations in syllable structure. Here, we recorded from the premotor nucleus robust nucleus of the arcopallium (RA) in Bengalese finches and measured whether neural activity covaried with syllable structure across multiple renditions of individual syllables. We found that variations in premotor activity were significantly correlated with variations in the acoustic features (pitch, amplitude, and spectral entropy) of syllables in approximately a quarter of all cases. In these cases, individual neural recordings predicted 8.5 Ϯ 0.3% (mean Ϯ SE) of the behavioral variation, and in some cases accounted for 25% or more of trial-by-trial variations in acoustic output. The prevalence and strength of neuron-behavior correlations indicate that each acoustic feature is controlled by a large ensemble of neurons that vary their activity in a coordinated manner. Additionally, we found that correlations with pitch (but not other features) were predominantly positive in sign, supporting a model of pitch production based on the anatomy and physiology of the vocal motor apparatus. Collectively, our results indicate that trial-by-trial variations in spectral structure are indeed under central neural control at the level of RA, consistent with the idea that such variation reflects motor exploration.
To successfully negotiate a cluttered environment, an echolocating bat must control the timing of motor behaviors in response to dynamic sensory information. Here we detail the big brown bat's adaptive temporal control over sonar call production for tracking prey, moving predictably or unpredictably, under different experimental conditions. We studied the adaptive control of vocal-motor behaviors in free-flying big brown bats, Eptesicus fuscus, as they captured tethered and free-flying insects, in open and cluttered environments. We also studied adaptive sonar behavior in bats trained to track moving targets from a resting position. In each of these experiments, bats adjusted the features of their calls to separate target and clutter. Under many task conditions, flying bats produced prominent sonar sound groups identified as clusters of echolocation pulses with relatively stable intervals, surrounded by longer pulse intervals. In experiments where bats tracked approaching targets from a resting position, bats also produced sonar sound groups, and the prevalence of these sonar sound groups increased when motion of the target was unpredictable. We hypothesize that sonar sound groups produced during flight, and the sonar call doublets produced by a bat tracking a target from a resting position, help the animal resolve dynamic target location and represent the echo scene in greater detail. Collectively, our data reveal adaptive temporal control over sonar call production that allows the bat to negotiate a complex and dynamic environment.
The control of sequenced behaviors, including human speech, requires that the brain coordinate the production of discrete motor elements with their concatenation into complex patterns. In birdsong, another sequential vocal behavior, the acoustic structure (phonology) of individual song elements, or "syllables," must be coordinated with the sequencing of syllables into a song. However, it is unknown whether syllable phonology is independent of the sequence in which a syllable is produced. We quantified interactions between phonology and sequence in Bengalese finch song by examining both convergent syllables, which can be preceded by at least two different syllables and divergent syllables, which can be followed by at least two different syllables. Phonology differed significantly based on the identity of the preceding syllable for 97% of convergent syllables and differed significantly with the identity of the upcoming syllable for 92% of divergent syllables. Furthermore, sequence-dependent phonological differences extended at least two syllables away from the convergent or divergent syllable. To determine whether these phenomena reflect differences in central control, we analyzed premotor neural activity in the robust nucleus of the arcopallium (RA). Activity associated with a syllable varied significantly depending on the sequence in which the syllable was produced, suggesting that sequence-dependent variations in premotor activity contribute to sequence-dependent differences in phonology. Moreover, these data indicate that RA activity could contribute to the sequencing of syllables. Together, these results suggest that, rather than being controlled independently, the sequence and phonology of birdsong are intimately related, as is the case for human speech.
Under natural conditions, animals encounter a barrage of sensory information from which they must select and interpret biologically relevant signals. Active sensing can facilitate this process by engaging motor systems in the sampling of sensory information. The echolocating bat serves as an excellent model to investigate the coupling between action and sensing because it adaptively controls both the acoustic signals used to probe the environment and movements to receive echoes at the auditory periphery. We report here that the echolocating bat controls the features of its sonar vocalizations in tandem with the positioning of the outer ears to maximize acoustic cues for target detection and localization. The bat’s adaptive control of sonar vocalizations and ear positioning occurs on a millisecond timescale to capture spatial information from arriving echoes, as well as on a longer timescale to track target movement. Our results demonstrate that purposeful control over sonar sound production and reception can serve to improve acoustic cues for localization tasks. This finding also highlights the general importance of movement to sensory processing across animal species. Finally, our discoveries point to important parallels between spatial perception by echolocation and vision.
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