RESUMEN
Auditory adaptation to sound-level statistics occurs as early as in the auditory nerve (AN), the first stage of neural auditory processing. In addition to firing rate adaptation characterized by a rate decrement dependent on previous spike activity, AN fibers show dynamic range adaptation, which is characterized by a shift of the rate-level function or dynamic range toward the most frequently occurring levels in a dynamic stimulus, thereby improving the precision of coding of the most common sound levels (Wen B, Wang GI, Dean I, Delgutte B. J Neurosci 29: 13797-13808, 2009). We investigated the time course of dynamic range adaptation by recording from AN fibers with a stimulus in which the sound levels periodically switch from one nonuniform level distribution to another (Dean I, Robinson BL, Harper NS, McAlpine D. J Neurosci 28: 6430-6438, 2008). Dynamic range adaptation occurred rapidly, but its exact time course was difficult to determine directly from the data because of the concomitant firing rate adaptation. To characterize the time course of dynamic range adaptation without the confound of firing rate adaptation, we developed a phenomenological "dual adaptation" model that accounts for both forms of AN adaptation. When fitted to the data, the model predicts that dynamic range adaptation occurs as rapidly as firing rate adaptation, over 100-400 ms, and the time constants of the two forms of adaptation are correlated. These findings suggest that adaptive processing in the auditory periphery in response to changes in mean sound level occurs rapidly enough to have significant impact on the coding of natural sounds.
Asunto(s)
Adaptación Fisiológica/fisiología , Nervio Coclear/fisiología , Modelos Biológicos , Dinámicas no Lineales , Estimulación Acústica , Potenciales de Acción/fisiología , Animales , Atención , Gatos , Lateralidad Funcional/fisiología , Psicoacústica , Factores de TiempoRESUMEN
The auditory system operates over a vast range of sound pressure levels (100-120 dB) with nearly constant discrimination ability across most of the range, well exceeding the dynamic range of most auditory neurons (20-40 dB). Dean et al. (2005) have reported that the dynamic range of midbrain auditory neurons adapts to the distribution of sound levels in a continuous, dynamic stimulus by shifting toward the most frequently occurring level. Here, we show that dynamic range adaptation, distinct from classic firing rate adaptation, also occurs in primary auditory neurons in anesthetized cats for tone and noise stimuli. Specifically, the range of sound levels over which firing rates of auditory nerve (AN) fibers grows rapidly with level shifts nearly linearly with the most probable levels in a dynamic sound stimulus. This dynamic range adaptation was observed for fibers with all characteristic frequencies and spontaneous discharge rates. As in the midbrain, dynamic range adaptation improved the precision of level coding by the AN fiber population for the prevailing sound levels in the stimulus. However, dynamic range adaptation in the AN was weaker than in the midbrain and not sufficient (0.25 dB/dB, on average, for broadband noise) to prevent a significant degradation of the precision of level coding by the AN population above 60 dB SPL. These findings suggest that adaptive processing of sound levels first occurs in the auditory periphery and is enhanced along the auditory pathway.
Asunto(s)
Estimulación Acústica/métodos , Estimulación Acústica/estadística & datos numéricos , Adaptación Fisiológica/fisiología , Percepción Auditiva/fisiología , Nervio Coclear/fisiología , Animales , Vías Auditivas/fisiología , Gatos , Tiempo de Reacción/fisiologíaRESUMEN
Auditory neurons must represent accurately a wide range of sound levels using firing rates that vary over a far narrower range of levels. Recently, we demonstrated that this "dynamic range problem" is lessened by neural adaptation, whereby neurons adjust their input-output functions for sound level according to the prevailing distribution of levels. These adjustments in input-output functions increase the accuracy with which levels around those occurring most commonly are coded by the neural population. Here, we examine how quickly this adaptation occurs. We recorded from single neurons in the auditory midbrain during a stimulus that switched repeatedly between two distributions of sound levels differing in mean level. The high-resolution analysis afforded by this stimulus showed that a prominent component of the adaptation occurs rapidly, with an average time constant across neurons of 160 ms after an increase in mean level, much faster than our previous experiments were able to assess. This time course appears to be independent of both the timescale over which sound levels varied and that over which sound level distributions varied, but is related to neural characteristic frequency. We find that adaptation to an increase in mean level occurs more rapidly than to a decrease. Finally, we observe an additional, slow adaptation in some neurons, which occurs over a timescale of tens of seconds. Our findings provide constraints in the search for mechanisms underlying adaptation to sound level. They also have functional implications for the role of adaptation in the representation of natural sounds.
Asunto(s)
Estimulación Acústica/métodos , Adaptación Fisiológica/fisiología , Sonido , Potenciales de Acción/fisiología , Animales , Percepción Auditiva/fisiología , Cobayas , Factores de TiempoRESUMEN
Mammals can hear sounds extending over a vast range of sound levels with remarkable accuracy. How auditory neurons code sound level over such a range is unclear; firing rates of individual neurons increase with sound level over only a very limited portion of the full range of hearing. We show that neurons in the auditory midbrain of the guinea pig adjust their responses to the mean, variance and more complex statistics of sound level distributions. We demonstrate that these adjustments improve the accuracy of the neural population code close to the region of most commonly occurring sound levels. This extends the range of sound levels that can be accurately encoded, fine-tuning hearing to the local acoustic environment.
Asunto(s)
Potenciales de Acción/fisiología , Percepción Auditiva/fisiología , Umbral Auditivo/fisiología , Colículos Inferiores/fisiología , Neuronas/fisiología , Transmisión Sináptica/fisiología , Estimulación Acústica , Animales , Vías Auditivas/fisiología , Cobayas , Percepción Sonora/fisiología , Percepción de la Altura Tonal/fisiología , Tiempo de Reacción/fisiología , Localización de Sonidos/fisiología , Factores de TiempoRESUMEN
We recorded a novel fast GABAergic synaptic current in cerebellar Purkinje cells in rat brain slices using patch-clamp techniques. Because of a relatively low sensitivity to bicuculline, these currents can be recorded under conditions in which basket and stellate cell inputs are blocked. The observations that the novel synaptic currents occur spontaneously only in the presence of serotonin, and the specific limited positions in the slice from which they can be electrically evoked, suggest that the presynaptic cell is the Lugaro cell. Cell-attached recordings confirm that the Lugaro cell is the only interneuron in the cerebellar cortex with firing behavior consistent with the spontaneous activity recorded in Purkinje cells. The input shows a strong presynaptic modulation mediated by GABA(A) receptors, resulting in a dynamic range from almost 0 to >90% release probability. Modeling GABA(A) receptor responses to different GABA transients suggests that the relatively low sensitivity of the synaptic currents to bicuculline, compared with the higher affinity GABA(A) receptor antagonist SR-95531 (2-(3-carboxypropyl)-3-amino-6-(4-methoxyphenyl) pyridazinium), is attributable to an unusually long GABA dwell time and/or high GABA concentration in the synaptic cleft. The significance of this novel input is discussed in relation to other GABAergic synapses impinging on Purkinje cells. We suggest that the release of GABA onto Purkinje cells from Lugaro cells would primarily occur during motor activity under conditions in which the activity of basket and stellate cells might be inhibited.
Asunto(s)
Cloruros/metabolismo , Células de Purkinje/metabolismo , Serotonina/fisiología , Sinapsis/metabolismo , Transmisión Sináptica/fisiología , Ácido gamma-Aminobutírico/metabolismo , Animales , Bicuculina/farmacología , Calcio/metabolismo , Células Cultivadas , Cerebelo/citología , Simulación por Computador , Relación Dosis-Respuesta a Droga , Antagonistas de Aminoácidos Excitadores/farmacología , Antagonistas de Receptores de GABA-A , Técnicas In Vitro , Modelos Neurológicos , Técnicas de Placa-Clamp , Células de Purkinje/citología , Células de Purkinje/efectos de los fármacos , Ratas , Ratas Sprague-Dawley , Receptores de GABA-A/metabolismo , Serotonina/farmacología , Sinapsis/efectos de los fármacos , Transmisión Sináptica/efectos de los fármacosRESUMEN
Precise refinement of synaptic connectivity is the result of activity-dependent mechanisms in which coincidence-dependent calcium signaling by NMDA receptors (NMDARs) under control of the voltage-dependent Mg2+ block might play a special role. In the developing rodent trigeminal system, the pattern of synaptic connections between whisker-specific inputs and their target cells in the brainstem is refined to form functionally and morphologically distinct units (barrelettes). To test the role of NMDA receptor signaling in this process, we introduced the N598R mutation into the native NR1 gene. This leads to the expression of functional NMDARs that are Mg2+ insensitive and Ca2+ impermeable. Newborn mice expressing exclusively NR1 N598R-containing NMDARs do not show any whisker-related patterning in the brainstem, whereas the topographic projection of trigeminal afferents and gross brain morphology appear normal. Furthermore, the NR1 N598R mutation does not affect expression levels of NMDAR subunits and other important neurotransmitter receptors. Our results show that coincidence detection by, and/or Ca2+ permeability of, NMDARs is necessary for the development of somatotopic maps in the brainstem and suggest that highly specific signaling underlies synaptic refinement.