Synaptic Mechanisms of Coincidence Detection

MacLeod, Katrina M.; Carr, Catherine E.

doi:10.1007/978-1-4419-9517-9_6

Cited by 9 publications

(11 citation statements)

References 127 publications

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“…Auditory brainstem circuitry is equipped with a suite of specializations to promote 23 coincidence detection [26]. Afferent inputs to MSO cells are reliable and 24 temporally-precise [27,28], dendritic processing in MSO further enhances coincidence 25 detection [25,[29][30][31], and voltage-gated currents that are partially active near resting 26 voltage make MSO cells extremely fast and precise processors [25,32].…”

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confidence: 99%

Soma-axon coupling configurations that enhance neuronal coincidence detection

Goldwyn

Remme

Rinzel

2018

Preprint

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Coincidence detector neurons transmit timing information by responding preferentially to concurrent synaptic inputs. Principal cells of the medial superior olive (MSO) in the mammalian auditory brainstem are superb coincidence detectors. They encode sound source location with high temporal precision, distinguishing submillisecond timing differences among inputs. We investigate computationally how dynamic coupling between the "input" region (soma and dendrite) and the spike-generating "output" region (axon and axon initial segment) can enhance coincidence detection in MSO neurons. To do this, we formulate a two-compartment neuron model and characterize extensively coincidence detection sensitivity throughout a parameter space of coupling configurations. We focus on the interaction between coupling configuration and two currents that provide dynamic, voltage-gated, negative feedback in subthreshold voltage range: sodium current with rapid inactivation and low-threshold potassium current, I KLT . These currents reduce synaptic summation and can prevent spike generation unless inputs arrive with near simultaneity. We show that strong soma-to-axon coupling promotes the negative feedback effects of sodium inactivation and is, therefore, advantageous for coincidence detection. Furthermore, the "feedforward" combination of strong soma-to-axon coupling and weak axon-to-soma coupling enables spikes to be generated efficiently (few sodium channels needed) and with rapid recovery that enhances high-frequency coincidence detection. These observations detail the functional benefit of the strongly feedforward configuration that has been observed in physiological studies of MSO neurons. We find that I KLT further enhances coincidence detection sensitivity, but with effects that depend on coupling configuration. For instance, in weakly-coupled models, I KLT in the spike-generator compartment enhances coincidence detection more effectively than I KLT in the input compartment. By using a minimal model of soma-to-axon coupling, we connect structure, dynamics, and computation. Here, we consider the particular case of MSO coincidence detectors. In principle, our method for creating and exploring a parameter space of two-compartment models can be applied to other neurons. PLOS1/30 Author summaryBrain cells (neurons) are spatially extended structures. The locations at which neurons receive inputs and generate outputs are often distinct. We formulate and study a minimal mathematical model that describes the dynamical coupling between the input and output regions of a neuron. We construct our model to reflect known properties of neurons in the auditory brainstem that play an important role in our ability to locate sound sources. These neurons are known as "coincidence detectors" because they are most likely to respond when they receive simultaneous inputs. We use simulations to explore coincidence detection sensitivity throughout the parameter space of input-output coupling and to identify the coupling configurations that are best for neu...

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Soma-axon coupling configurations that enhance neuronal coincidence detection

Goldwyn

Remme

Rinzel

2018

Preprint

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“…Short‐term plasticity of EPSCs is particularly important for auditory brainstem processing (MacLeod & Carr, ). While both synaptic depression and facilitation are present in the part of cochlear nucleus neurons that encodes intensity information among other sound features (MacLeod et al .…”

Section: Resultsmentioning

confidence: 99%

“…2C and D; ipsi rise time: 0.603 ± 0.093 ms, contra rise time: 0.599 ± 0.082 ms, paired t test P = 0.890; ipsi decay tau: 1.563 ± 0.178 ms, contra decay tau: 1.659 ± 0.260 ms, paired t test P = 0.567, n = 37). Short-term plasticity of EPSCs is particularly important for auditory brainstem processing (MacLeod & Carr, 2012). While both synaptic depression and facilitation are present in the part of cochlear nucleus neurons that encodes intensity information among other sound features (MacLeod et al 2007), strong synaptic depression dominates in the timing-coding NM neurons.…”

Section: Symmetry In Physiology Between the Bilateral Excitatory Inpumentioning

confidence: 99%

Activity‐dependent synaptic integration and modulation of bilateral excitatory inputs in an auditory coincidence detection circuit

Liu

Curry

2018

The Journal of Physiology

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Neurons in the avian nucleus laminaris (NL) receive bilateral excitatory inputs from the cochlear nucleus magnocellularis, via morphologically symmetrical dorsal (ipsilateral) and ventral (contralateral) dendrites. Using in vitro whole-cell patch recordings in chicken brainstem slices, we investigated synaptic integration and modulation of the bilateral inputs to NL under normal and hearing deprivation conditions. We found that the two excitatory inputs onto single NL neurons were nearly completely segregated, and integration of the two inputs was linear for EPSPs. The two inputs had similar synaptic strength, kinetics and short-term plasticity. EPSCs in low but not middle and high frequency neurons were suppressed by activation of group I and II metabotropic glutamate receptors (mGluR I and II), with similar modulatory strength between the ipsilateral and contralateral inputs. Unilateral hearing deprivation by cochlea removal reduced the excitatory transmission on the deprived dendritic domain of NL. Interestingly, EPSCs evoked at the deprived domain were modulated more strongly by mGluR II than at the counterpart domain that received intact input in low frequency neurons, suggesting anti-homeostatic regulation. This was supported by a stronger expression of mGluR II protein on the deprived neuropils of NL. Under mGluR II modulation, EPSCs on the deprived input show transient synaptic facilitation, forming a striking contrast with normal hearing conditions under which pure synaptic depression is observed. These results demonstrate physiological symmetry and thus balanced bilateral excitatory inputs to NL neurons. The activity-dependent anti-homeostatic plasticity of mGluR modulation constitutes a novel mechanism regulating synaptic transmission in response to sensory input manipulations.

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“…The average IV curve was linear (ohmic; dashed line) over a range of negative current with a slope (input resistance) R m = 207 MΩ (Figure 3B). Deviations from linearity are due to activation of I KLT for positive currents and I h for negative currents (Brew and Forsythe, 1995;MacLeod and Carr, 2012). For small current injections, the average R m = 247 ± 65 MΩ (n=6; P20).…”

Section: Previous Morphological Reconstructions Of Mntb Principal Celmentioning

confidence: 99%

“…Specialized time-coding auditory brainstem neurons can have very low R i and fast τ M (Scott et al, 2005). In fact, some avian and mammalian neurons can have an extremely fast EPSP time course that is nearly identical to that of the EPSC (MacLeod and Carr, 2012).…”

Section: Introduction (631<650 Words)mentioning

confidence: 99%