Mammalian octopus cells are direction selective to frequency sweeps by excitatory synaptic sequence detection

Lu, Hsin-Wei; Smith, Philip H.; Joris, Philip X.

doi:10.1073/pnas.2203748119

Cited by 17 publications

(24 citation statements)

References 85 publications

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“…As an example, octopus cells (Fig. 1) only detect (fire in response to) coincident firing of large groups of AN fibers, while the pure tone used here is a very poor stimulus for these cells (Ferragamo and Oertel, 2002;Smith et al, 2005;Liu et al, 2022). In contrast, octopus cells respond very robustly and accurately to click stimuli at high rates while other VCN neurons do not.…”

Section: Hvos Imaging With Train Stimulationmentioning

confidence: 89%

“…Octopus cells were not labeled, presumably because their pure tone thresholds are high (Godfrey et al, 1975;Rhode and Smith, 1986). Also, if they did respond, they would only fire a single onset spike to the stimuli we used (Rhode et al, 1983;Oertel et al, 2000;Smith et al, 2005;McGinley et al, 2012;Liu et al, 2022), which would presumably be less effective in driving probe expression. The small cell cap, a region that receives both auditory and somatosensory input (Shore and Zhou, 2006), also contained TRAP-labeled neurons (* in Figs.…”

Section: Labeling Of Isofrequency Bandsmentioning

confidence: 99%

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Imaging Voltage Globally and in Isofrequency Lamina in Slices of Mouse Ventral Cochlear Nucleus

Shu²,

Lin³

et al. 2023

eNeuro

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The cochlear nuclei (CN) receive sensory information from the ear and perform fundamental computations before relaying this information to higher processing centers. These computations are performed by distinct types of neurons interconnected in circuits dedicated to the specialized roles of the auditory system. In the present study we explored the use of voltage imaging to investigate CN circuitry. We tested two approaches based on fundamentally different voltage sensing technologies. Using a voltage-sensitive dye we recorded glutamate receptor-independent signals arising predominantly from axons. The mean conduction velocity of these fibers of 0.27 m/sec was rapid but in range with other unmyelinated axons. We then used a genetically-encoded hybrid voltage sensor (hVOS) to image voltage from a specific population of neurons. Probe expression was controlled using Cre recombinase linked toc-fosactivation. This activity-induced gene enabled targeting of neurons that are activated when a mouse hears a pure 15 kHz tone. In CN slices from these animals auditory nerve fiber stimulation elicited a glutamate receptor-dependent depolarization in hVOS probe-labeled neurons. These cells resided within a band corresponding to an isofrequency lamina, and responded with a high degree of synchrony. In contrast to the axonal origin of voltage-sensitive dye signals, hVOS signals represent predominantly post-synaptic responses. The introduction of voltage imaging to the CN creates the opportunity to investigate auditory processing circuitry in populations of neurons targeted on the basis of their genetic identity and their roles in sensory processing.Significance StatementThe cochlear nucleus uses dedicated circuitry to process and interpret information from the ear. This circuitry is organized tonotopically into laminae, each containing cells with an optimal sensitivity to a specific sound frequency. By targeting a genetically-encoded hybrid voltage sensor (hVOS) to identify neurons activated during the presentation of sound, the properties and function of these neurons become accessible to study in slices of mouse ventral cochlear nucleus. Imaging hVOS signals in these slices recapitulated the tonotopic organization. Imaging with a voltage sensitive dye provided a contrasting global view of signals arising predominantly from unmyelinated axons creating a potential method for studying type II auditory nerve or DCN parallel fibers.

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Section: Hvos Imaging With Train Stimulationmentioning

confidence: 89%

Section: Labeling Of Isofrequency Bandsmentioning

confidence: 99%

Imaging Voltage Globally and in Isofrequency Lamina in Slices of Mouse Ventral Cochlear Nucleus

Shu²,

Lin³

et al. 2023

eNeuro

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“…On the other hand, it seems likely that “across-CF” combinations of excitatory and inhibitory inputs to IC neurons, with different timing, could produce neural sensitivity to sweep direction (Gittelman et al, 2009; Suga, 1965), or at least influence sweep sensitivity, potentially explaining differences in Schroeder bias observed between IC neurons of similar CF. Multiple excitatory inputs from auditory-nerve inputs with different CFs produces direction selectivity for frequency sweeps in octopus cells of the mammalian cochlear nucleus (Lu et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

Mechanisms of masking by Schroeder-phase harmonic tone complexes in the budgerigar (Melopsittacus undulatus)

Henry

Wang

Abrams

et al. 2022

Preprint

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Schroeder-phase harmonic tone complexes have a flat temporal envelope and either rising or falling instantaneous frequency sweeps within F0 periods, depending on the polarity of the phase-scaling parameter C. Human thresholds for detection of a pure-tone target added to a Schroeder HTC can be 10-15 dB lower for the positive Schroeder (downward-sweeping) compared to negative (upward-sweeping), potentially due to the impulse response of the basilar membrane though this hypothesis remains controversial. Specifically, the upward-gliding impulse response observed empirically in several studies is expected to produce a peakier envelope response for positive Schroeder HTCs, thereby reducing masking compared to negative Schroeder HTCs. Birds provide an interesting animal model for studying Schroeder masking because prior studies suggest less behavioral threshold difference between Schroeder maskers of opposite polarity. However, neurophysiological mechanisms have not been explored and previous behavioral studies mostly used Schroeder HTCs with relatively low F0s. To gain further insight into underlying Schroeder masking mechanisms, we performed operant-conditioning experiments in budgerigars (Melopsittacus undulatus), a parakeet species, using a wide range of F0 and C values. Awake neurophysiological recordings in the avian inferior colliculus, a major envelope processing station in the midbrain, characterized neural encoding of behavioral test stimuli. Behavioral Schroeder masking thresholds increased with increasing F0 and showed minimal difference between opposite Schroeder polarities for all conditions, similar to prior studies in this and other bird species. Neural recordings showed prominent temporal and average-rate-based encoding of Schroeder F0, and in many neurons, marked response asymmetries between opposite Schroeder polarities. While response bias varied considerably across neurons, average bias of the population shifted from negative to positive with increasing characteristic frequency, with a breakpoint at ~2-3 kHz. Response bias was weakly associated with lower Schroeder-masked tone detection of neurons for the 400-Hz F0 only. These results challenge the common assumption that a peakier masker response results in a lower threshold for target tone detection with this paradigm.

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Section: Significancementioning

confidence: 99%

“…Rate-differences between SCHR direction may be partially explained by the phase-dispersive properties in the cochlea (Recio and Rhode, 2000), which might combine with cochlear compression to result in reduced responses to downward-sweeping SCHR chirps in the auditory nerve (AN), at least for the highfrequency region (Recio, 2001). Chirp selectivity in the IC could also arise in octopus cells of the cochlear nucleus, which are selective to SCHR chirp direction (Lu et al, 2022) and provide inhibition to the IC via the ventral nucleus of the lateral lemniscus (VNLL) (Adams, 1997).Alternatively, chirp selectivity may originate (or be influenced) at the level of the IC by the same or similar mechanisms that give rise to other complex stimulus sensitivities. For instance, IC tuning for periodicity (Langner and Schreiner, 1988;Krishna and Semple, 2000;Nelson and Carney, 2007;Kim et al, 2020) can be explained by the dynamics of inhibitory inputs (Nelson and Carney, 2004).…”

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confidence: 99%

Sensitivity to direction and velocity of fast frequency chirps in the inferior colliculus of awake rabbit

Mitchell

Carney

2022

Preprint

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Neurons in the rabbit inferior colliculus (IC) are selective for the direction of fast frequency chirps (frequency sweeps) contained in Schroeder-Harmonic Complexes (SCHR). This selectivity may point to a feature sensitivity to fast chirp direction and velocity in the IC shared by all mammals. Here, we introduce a novel stimulus consisting of Aperiodic Random Chirps (ARC) to distinguish neurons′ sensitivity to chirp direction and velocity from the confounding periodicity of SCHR stimuli. Extracellular, single-unit recordings were made in the IC of five Dutch-belted rabbits. SCHR stimuli were presented at a range of velocities and periodicities. Corresponding ARC stimuli and sinsuoidally amplitude-modulated (SAM) noise were also presented. The prevalence of direction selectivity and direction bias of selectivity to chirps in SCHR and ARC responses was quantified, revealing that the majority of IC neurons (90.3%) are selective to chirp direction. Additionally, although this selectivity was biased for negative SCHR chirp directions, neurons with both positive and negative biases for every SCHR and ARC condition were observed. Modulation-transfer-function type was not significantly related to chirp selectivity, but characteristic frequency was related to both the prevalence of direction selectivity and direction bias of chirp responses. Responses to ARC and SAM noise stimuli were used as input to a generalized linear model (GLM) to predict SCHR responses rates, based on the premise that ARC and SAM noise responses correspond to neurons′ velocity and periodicity response profiles, respectively. The results of the GLM analysis reveal that velocity-terms represented a substantial percentage of the total explainable variance, over 50% for some neurons. We discuss how chirp direction and velocity sensitivity may have implications for midbrain-level encoding of speech.

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Mammalian octopus cells are direction selective to frequency sweeps by excitatory synaptic sequence detection

Cited by 17 publications

References 85 publications

Imaging Voltage Globally and in Isofrequency Lamina in Slices of Mouse Ventral Cochlear Nucleus

Imaging Voltage Globally and in Isofrequency Lamina in Slices of Mouse Ventral Cochlear Nucleus

Mechanisms of masking by Schroeder-phase harmonic tone complexes in the budgerigar (Melopsittacus undulatus)

Sensitivity to direction and velocity of fast frequency chirps in the inferior colliculus of awake rabbit

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