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Bennett, M. M.

Publications and source records attributed to Bennett, M. M..

4 recordsLinked to original sources

Divergent co-transmission by a predictive motor circuit modulates auditory processing.

During behavior, an animals movements often stimulate its own sensory receptors. For instance, whether during flight or the production of courtship song, when flies beat their wings they cause mechanosensory disturbances that activate primary auditory neurons in the antennae. However, flight and courtship occur under very different behavioral contexts and temporal-scales. As a consequence, the nervous system contains predictive motor circuits that modify sensory processing in anticipation of self-induced (re-afferent) stimulation. However, it is unclear how information about planned movements can be used to effectively tune specialized sensory processing circuits. Here we describe a predictive motor circuit that releases two transmitters to differentially modify auditory neurons that process sound under different behavioral contexts. In Drosophila, two metathoracic ascending histamine neurons (MtAHNs) become active prior to wing movement and project to the primary auditory network. We found that the MtAHNs co-transmit the neuropeptide Dh44 and histamine, and each suppresses the activity of auditory neurons that are integrated into distinct networks that support escape and courtship, respectively. Additionally, Dh44 has a greater impact on male auditory neurons and suppression by Dh44 occurs over a longer time course than histamine. Disrupting either histamine synthesis or neuropeptide release by the MtAHNs reduces courtship success with an increase in cessation during the wing extension step. Consistent with a role in auditory processing of courtship cues, Dh44 cotransmission is present in Drosophila species that have an auditory component to their courtship displays, but is absent in species that use either purely visual courtship or lack apparent courtship behavior. Finally, the projections of the MtAHNs into auditory centers were missing in snow flies, which are wingless. Our results indicate that divergent cotransmission by predictive motor circuits may represent an efficient means to differentially modulate sensory subnetworks impacted by reafferent feedback.

neuroscience↗

Connectivity of serotonin neurons reveals a constrained inhibitory subnetwork within the olfactory system.

Inhibitory local interneurons (LNs) play an essential role in sensory processing by refining stimulus representations via a diverse collection of mechanisms. The morphological and physiological traits of individual LN types, as well as their connectivity within sensory networks, enable each LN type to support different computations such as lateral inhibition or gain control and are therefore ideal targets for modulatory neurons to have widespread impacts on network activity. In this study, we combined detailed connectivity analyses, serotonin receptor expression, neurophysiology, and computational modeling to demonstrate the functional impact of serotonin on a constrained LN network in the olfactory system of Drosophila. This subnetwork is composed of three LN types and we describe each of their distinctive morphology, connectivity, biophysical properties and odor response properties. We demonstrate that each LN type expresses different combinations of serotonin receptors and that serotonin differentially impacts the excitability of each LN type. Finally, by applying these serotonin induced changes in excitability to a computational model that simulates the impact of inhibition exerted by each LN-type, we predict a role for serotonin in adjusting the dynamic range of antennal lobe output neurons and in noise reduction in odor representations. Thus, a single modulatory system can differentially impact LN types that subserve distinct roles within the olfactory system. Significance StatementInhibitory interneurons refine information processing within sensory networks by enforcing distinct local computations. They are therefore ideal targets for modulatory neurons to efficiently alter sensory processing by up- or downregulating the computations each interneuron class subserves. We identify an interconnected network of three interneuron types in the olfactory system of Drosophila that receive a large amount of serotonergic synaptic input. Each interneuron type differs in their biophysical and response properties and serotonin differentially impacts their excitability. Finally, using a computational model, we predict that the combined effects of serotonin on these inhibitory neurons enables noise reduction in the olfactory system. Thus, modulation of individual cell types collectively adjusts distinct network computations to enable flexible sensory coding.

neuroscience↗

Organization of an Ascending Circuit that Conveys Flight Motor State

Natural behaviors are a coordinated symphony of motor acts which drive self-induced or reafferent sensory activation. Single sensors only signal presence and magnitude of a sensory cue; they cannot disambiguate exafferent (externally-induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to make appropriate decisions and initiate adaptive behavioral outcomes. This is mediated by predictive motor signaling mechanisms, which emanate from motor control pathways to sensory processing pathways, but how predictive motor signaling circuits function at the cellular and synaptic level is poorly understood. We use a variety of techniques, including connectomics from both male and female electron microscopy volumes, transcriptomics, neuroanatomical, physiological and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs), which putatively provide predictive motor signals to several sensory and motor neuropil. Both AHN pairs receive input primarily from an overlapping population of descending neurons, many of which drive wing motor output. The two AHN pairs target almost exclusively non-overlapping downstream neural networks including those that process visual, auditory and mechanosensory information as well as networks coordinating wing, haltere, and leg motor output. These results support the conclusion that the AHN pairs multi-task, integrating a large amount of common input, then tile their output in the brain, providing predictive motor signals to non-overlapping sensory networks affecting motor control both directly and indirectly.

neuroscience↗

Soldier neural architecture is temporarily modality-specialized but poorly predicted by repertoire size in the stingless bee Tetragonisca angustula

Individual heterogeneity within societies provides opportunities to test hypotheses about adaptive neural investment in the context of group cooperation. Here we explore neural investment in defense specialist soldiers of the eusocial stingless bee (Tetragonisca angustula) which are age sub-specialized on distinct defense tasks, and have an overall higher lifetime task repertoire than other sterile workers within the colony. Consistent with predicted behavioral demands, soldiers had higher relative visual (optic lobe) investment than non-soldiers but only during the period when they were performing the most visually demanding defense task (hovering guarding). As soldiers aged into the less visually demanding task of standing guarding this difference disappeared. Neural investment was otherwise similar across all colony members. Despite having larger task repertoires, soldiers had similar absolute brain size and smaller relative brain size compared to other workers, meaning that lifetime task repertoire size was a poor predictor of brain size. Together, our results are consistent with the specialized but flexible defense strategies of this species, broadening our understanding of how neurobiology mediates age and morphological task specialization in highly cooperative societies.

neuroscience↗