How do sensory systems optimize detection of behaviorally relevant stimuli when the sensory environment is constantly changing? We addressed the role of spike timing-dependent plasticity (STDP) in driving changes in synaptic strength in a sensory pathway and whether those changes in synaptic strength could alter sensory tuning. It is challenging to precisely control temporal patterns of synaptic activity in vivo and replicate those patterns in vitro in behaviorally relevant ways. This makes it difficult to make connections between STDP-induced changes in synaptic physiology and plasticity in sensory systems. Using the mormyrid species Brevimyrus niger and Brienomyrus brachyistius, which produce electric organ discharges for electrolocation and communication, we can precisely control the timing of synaptic input in vivo and replicate these same temporal patterns of synaptic input in vitro. In central electrosensory neurons in the electric communication pathway, using whole cell intracellular recordings in vitro, we paired presynaptic input with postsynaptic spiking at different delays. Using whole cell intracellular recordings in awake, behaving fish, we paired sensory stimulation with postsynaptic spiking using the same delays. We found that Hebbian STDP predictably alters sensory tuning in vitro and is mediated by NMDA receptors. However, the change in synaptic responses induced by sensory stimulation in vivo did not adhere to the direction predicted by the STDP observed in vitro. Further analysis suggests that this difference is influenced by polysynaptic activity, including inhibitory interneurons. Our findings suggest that STDP rules operating at identified synapses may not drive predictable changes in sensory responses at the circuit level. NEW & NOTEWORTHY We replicated behaviorally relevant temporal patterns of synaptic activity in vitro and used the same patterns during sensory stimulation in vivo. There was a Hebbian spike timing-dependent plasticity (STDP) pattern in vitro, but sensory responses in vivo did not shift according to STDP predictions. Analysis suggests that this disparity is influenced by differences in polysynaptic activity, including inhibitory interneurons. These results suggest that STDP rules at synapses in vitro do not necessarily apply to circuits in vivo.
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Generalization of learned responses in the mormyrid electrosensory lobe
Appropriate generalization of learned responses to new situations is vital for adaptive behavior. We provide a circuit-level account of generalization in the electrosensory lobe (ELL) of weakly electric mormyrid fish. Much is already known in this system about a form of learning in which motor corollary discharge signals cancel responses to the uninformative input evoked by the fish’s own electric pulses. However, for this cancellation to be useful under natural circumstances, it must generalize accurately across behavioral regimes, specifically different electric pulse rates. We show that such generalization indeed occurs in ELL neurons, and develop a circuit-level model explaining how this may be achieved. The mechanism involves regularized synaptic plasticity and an approximate matching of the temporal dynamics of motor corollary discharge and electrosensory inputs. Recordings of motor corollary discharge signals in mossy fibers and granule cells provide direct evidence for such matching.
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- Award ID(s):
- 1707398
- NSF-PAR ID:
- 10099423
- Date Published:
- Journal Name:
- eLife
- Volume:
- 8
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Sensory feedback during movement entails sensing a mix of externally- and self-generated stimuli (respectively, exafference and reafference). In many peripheral sensory systems, a parallel copy of the motor command, a corollary discharge, is thought to eliminate sensory feedback during behaviors. However, reafference has important roles in motor control, because it provides real-time feedback on the animal’s motions through the environment. In this case, the corollary discharge must be calibrated to enable feedback while avoiding negative consequences like sensor fatigue. The undulatory motions of fishes’ bodies generate induced flows that are sensed by the lateral line sensory organ, and prior work has shown these reafferent signals contribute to the regulation of swimming kinematics. Corollary discharge to the lateral line reduces the gain for reafference, but cannot eliminate it altogether. We develop a data-driven model integrating swimming biomechanics, hair cell physiology, and corollary discharge to understand how sensory modulation is calibrated during locomotion in larval zebrafish. In the absence of corollary discharge, lateral line afferent units exhibit the highly heterogeneous habituation rates characteristic of hair cell systems, typified by decaying sensitivity and phase distortions with respect to an input stimulus. Activation of the corollary discharge prevents habituation, reduces response heterogeneity, and regulates response phases in a narrow interval around the time of the peak stimulus. This suggests a synergistic interaction between the corollary discharge and the polarization of lateral line sensors, which sharpens sensitivity along their preferred axes. Our integrative model reveals a vital role of corollary discharge for ensuring precise feedback, including proprioception, during undulatory locomotion.more » « less
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Electroreception, the capacity to detect external underwater electric fields with specialised receptors, is a phylogenetically widespread sensory modality in fishes and amphibians. In passive electroreception, a capacity possessed by
c . 16% of fish species, an animal uses low‐frequency‐tuned ampullary electroreceptors to detect microvolt‐range bioelectric fields from prey, without the need to generate its own electric field. In active electroreception (electrolocation), which occurs only in the teleost lineages Mormyroidea and Gymnotiformes, an animal senses its surroundings by generating a weak (< 1 V) electric‐organ discharge (EOD) and detecting distortions in the EOD‐associated field using high‐frequency‐tuned tuberous electroreceptors. Tuberous electroreceptors also detect the EODs of neighbouring fishes, facilitating electrocommunication. Several other groups of elasmobranchs and teleosts generate weak (< 10 V) or strong (> 50 V) EODs that facilitate communication or predation, but not electrolocation. Approximately 1.5% of fish species possess electric organs. This review has two aims. First, to synthesise our knowledge of the functional biology and phylogenetic distribution of electroreception and electrogenesis in fishes, with a focus on freshwater taxa and with emphasis on the proximate (morphological, physiological and genetic) bases of EOD and electroreceptor diversity. Second, to describe the diversity, biogeography, ecology and electric signal diversity of the mormyroids and gymnotiforms and to explore the ultimate (evolutionary) bases of signal and receptor diversity in their convergent electrogenic–electrosensory systems. Four sets of potential drivers or moderators of signal diversity are discussed. First, selective forces of an abiotic (environmental) nature for optimal electrolocation and communication performance of the EOD. Second, selective forces of a biotic nature targeting the communication function of the EOD, including sexual selection, reproductive interference from syntopic heterospecifics and selection from eavesdropping predators. Third, non‐adaptive drift and, finally, phylogenetic inertia, which may arise from stabilising selection for optimal signal‐receptor matching. -
Baden, Tom (Ed.)Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal’s awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes’ undulatory body motions induce reafferent feedback that can encode the body’s instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors’ preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.more » « less
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Abstract Negative correlations in the sequential evolution of interspike intervals (ISIs) are a signature of memory in neuronal spike-trains. They provide coding benefits including firing-rate stabilization, improved detectability of weak sensory signals, and enhanced transmission of information by improving signal-to-noise ratio. Primary electrosensory afferent spike-trains in weakly electric fish fall into two categories based on the pattern of ISI correlations: non-bursting units have negative correlations which remain negative but decay to zero with increasing lags (Type I ISI correlations), and bursting units have oscillatory (alternating sign) correlation which damp to zero with increasing lags (Type II ISI correlations). Here, we predict and match observed ISI correlations in these afferents using a stochastic dynamic threshold model. We determine the ISI correlation function as a function of an arbitrary discrete noise correlation function
$${{\,\mathrm{\mathbf {R}}\,}}_k$$ k is a multiple of the mean ISI. The function permits forward and inverse calculations of the correlation function. Both types of correlation functions can be generated by adding colored noise to the spike threshold with Type I correlations generated with slow noise and Type II correlations generated with fast noise. A first-order autoregressive (AR) process with a single parameter is sufficient to predict and accurately match both types of afferent ISI correlation functions, with the type being determined by the sign of the AR parameter. The predicted and experimentally observed correlations are in geometric progression. The theory predicts that the limiting sum of ISI correlations is$$-0.5$$ $$-0.475 \pm 0.04$$ $$\text {mean} \pm \text {s.d.}$$
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7554/eLife.44032
