Lemniscal recurrent and transcortical influences on cuneate neurons

[Abstract] Intracellular recordings were obtained from cuneate neurons of chloralose-anesthetized, paralysed cats to study the synaptic responses induced by electrical stimulation of the contralateral medial lemniscus. From a total of 178 cells sampled, 109 were antidromically fired from the medial lemniscus, 82 of which showed spontaneous bursting activity. In contrast, the great majority (58/69) of the non-lemniscal neurons presented spontaneous single spike activity. Medial lemniscus stimulation induced recurrent excitation and inhibition on cuneolemniscal and non-lemniscal cells. Some non-lemniscal neurons were activated by somatosensory cortex and inhibited by motor cortex stimulation. Some other non-lemniscal cells that did not respond to medial lemniscus stimulation in control conditions were transcortically affected by stimulating the medial lemniscus after inducing paroxysmal activity in the sensorimotor cortex. These findings indicate that different sites in the sensorimotor cortex can differentially influence the sensory transmission through the cuneate, and that the distinct available corticocuneate routes are selected within the cerebral cortex. From a total of 92 cells tested, the initial effect induced by low-frequency stimulation of the sensorimotor cortex was inhibition on most of the cuneolemniscal neurons (32/52) and excitation on the majority of the non-lemniscal cells (25/40). The fact that a substantial proportion of cuneolemniscal and non-lemniscal cells was excited and inhibited, respectively, suggests that the cerebral cortex may potentiate certain inputs by exciting and disinhibiting selected groups of cuneolemniscal cells. Finally, evidence is presented demonstrating that the tendency of the cuneolemniscal neurons to fire in high-frequency spike bursts is due to different mechanisms, including excitatory synaptic potentials, recurrent activation through lemniscal axonal collaterals, and via the lemnisco-thalamo-cortico-cuneate loop. A corticocuneate network circuit to explain the results is proposed.Dirección General de Investigación Científica y Técnica; PB96-095

Corticofugal Gating of Auditory Information in the Thalamus: An In Vivo Intracellular Recording Study

In the present study, we investigated the auditory responses of the medial geniculate (MGB) neurons, through in vivo intracellular recordings of anesthetized guinea pigs, while the auditory cortex was electrically activated. Of the 63 neurons that received corticofugal modulation of the membrane potential, 30 received potentiation and 33 received hyperpolarization. The corticofugal potentiation of the membrane potential (amplitude, mean ± SD, 8.6 ± 5.5 mV; duration, 125.5 ± 75.4 msec) facilitated the auditory responses and spontaneous firing of the MGB neurons. The hyperpolarization of -11.3 ± 4.9 mV in amplitude and 210.0 ± 210. 1 msec in duration suppressed the auditory responses and spontaneous firing of the MGB neurons. Four of the five neurons that were histologically confirmed to be located in the lemniscal MGB received corticofugal facilitatory modulation, and all of the four neurons that were confirmed to be located in the non-lemniscal MGB received corticofugal inhibitory modulation. The present intracellular recording provides novel results on how the corticofugal projection gates the sensory information in the thalamus: via the spatially selective depolarization of lemniscal MGB neurons and hyperpolarization of non-lemniscal MGB neurons. It is speculated that the systematic selectivity of facilitation and inhibition over the lemniscal and non-lemniscal MGB is related to the attention shift within the auditory modality and across the sensory modalities.published_or_final_versio

Cholinergic modulation of stimulus-specific adaptation and prediction error responses in the auditory cortex of the rat

[ES]En esta tesis, describiré las respuestas generales a la adaptación específica a estímulos en la corteza auditiva de rata. A continuación, describiré cómo la acetilcolina modula esta respuesta frente a estímulos novedosos, cuáles son los receptores colinérgicos asociados a esta modulación y además mostraré cómo la acetilcolina modula los niveles de predicción de error. Finalmente, describiremos cómo las ratas pueden discriminar sonidos novedosos relevantes para el comportamient

Deviance detection in auditory subcortical structures: what can we learn from neurochemistry and neural connectivity?

[EN] A remarkable ability of animals that is critical for survival is to detect and respond to to unexpected stimuli in an ever-changing world. Auditory neurons that show stimulusspecific adaptation (SSA), i.e., a decrease in their response to frequently occurring stimuli while maintaining responsiveness when different stimuli are presented, might participate in the coding of deviance occurrence. Traditionally, deviance detection is measured by the mismatch negativity (MMN) potential in studies of evoked local field potentials.We present a review of the state-of-the-art of SSA in auditory subcortical nuclei, i.e., the inferior colliculus and medial geniculate body of the thalamus, and link the differential receptor distribution and neural connectivity of those regions in which extreme SSA has been found. Furthermore, we review both SSA and MMN-like responses in auditory and non-auditory areas that exhibit multimodal sensitivities that we suggest conform to a distributed network encoding for deviance detection. The understanding of the neurochemistry and response similarities across these different regions will contribute to a better understanding of the neural mechanism underlying deviance detection

Neurons along the auditory pathway exhibit a hierarchical organization of prediction error

Perception is characterized by a reciprocal exchange of predictions and prediction error signals between neural regions. However, the relationship between such sensory mismatch responses and hierarchical predictive processing has not yet been demonstrated at the neuronal level in the auditory pathway. We recorded single-neuron activity from different auditory centers in anaesthetized rats and awake mice while animals were played a sequence of sounds, designed to separate the responses due to prediction error from those due to adaptation effects. Here we report that prediction error is organized hierarchically along the central auditory pathway. These prediction error signals are detectable in subcortical regions and increase as the signals move towards auditory cortex, which in turn demonstrates a large-scale mismatch potential. Finally, the predictive activity of single auditory neurons underlies automatic deviance detection at subcortical levels of processing. These results demonstrate that prediction error is a fundamental component of singly auditory neuron responses

Stimulus-Specific Adaptation in the Auditory Thalamus of the Anesthetized Rat

The specific adaptation of neuronal responses to a repeated stimulus (Stimulus-specific adaptation, SSA), which does not fully generalize to other stimuli, provides a mechanism for emphasizing rare and potentially interesting sensory events. Previous studies have demonstrated that neurons in the auditory cortex and inferior colliculus show SSA. However, the contribution of the medial geniculate body (MGB) and its main subdivisions to SSA and detection of rare sounds remains poorly characterized. We recorded from single neurons in the MGB of anaesthetized rats while presenting a sequence composed of a rare tone presented in the context of a common tone (oddball sequences). We demonstrate that a significant percentage of neurons in MGB adapt in a stimulus-specific manner. Neurons in the medial and dorsal subdivisions showed the strongest SSA, linking this property to the non-lemniscal pathway. Some neurons in the non-lemniscal regions showed strong SSA even under extreme testing conditions (e.g., a frequency interval of 0.14 octaves combined with a stimulus onset asynchrony of 2000 ms). Some of these neurons were able to discriminate between two very close frequencies (frequency interval of 0.057 octaves), revealing evidence of hyperacuity in neurons at a subcortical level. Thus, SSA is expressed strongly in the rat auditory thalamus and contribute significantly to auditory change detection

Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus

[EN] Auditory neurons that exhibit stimulus-specific adaptation (SSA) decrease their response to common tones while retaining responsiveness to rare ones. We recorded single-unit responses from the inferior colliculus (IC) where SSA is known to occur and we explored for the first time SSA in the cochlear nucleus (CN) of rats. We assessed an important functional outcome of SSA, the extent to which frequency discriminability depends on sensory context. For this purpose, pure tones were presented in an oddball sequence as standard (high probability of occurrence) or deviant (low probability of occurrence) stimuli. To study frequency discriminability under different probability contexts, we varied the probability of occurrence and the frequency separation between tones. The neuronal sensitivity was estimated in terms of spike-count probability using signal detection theory. We reproduced the finding that many neurons in the IC exhibited SSA, but we did not observe significant SSA in our CN sample. We concluded that strong SSA is not a ubiquitous phenomenon in the CN. As predicted, frequency discriminability was enhanced in IC when stimuli were presented in an oddball context, and this enhancement was correlated with the degree of SSA shown by the neurons. In contrast, frequency discrimination by CN neurons was independent of stimulus context. Our results demonstrated that SSA is not widespread along the entire auditory pathway, and suggest that SSA increases frequency discriminability of single neurons beyond that expected from their tuning curves

Adjudicating between local and global architectures of predictive processing in the subcortical auditory pathway

Predictive processing, a leading theoretical framework for sensory processing, suggests that the brain constantly generates predictions on the sensory world and that perception emerges from the comparison between these predictions and the actual sensory input. This requires two distinct neural elements: generative units, which encode the model of the sensory world; and prediction error units, which compare these predictions against the sensory input. Although predictive processing is generally portrayed as a theory of cerebral cortex function, animal and human studies over the last decade have robustly shown the ubiquitous presence of prediction error responses in several nuclei of the auditory, somatosensory, and visual subcortical pathways. In the auditory modality, prediction error is typically elicited using so-called oddball paradigms, where sequences of repeated pure tones with the same pitch are at unpredictable intervals substituted by a tone of deviant frequency. Repeated sounds become predictable promptly and elicit decreasing prediction error; deviant tones break these predictions and elicit large prediction errors. The simplicity of the rules inducing predictability make oddball paradigms agnostic about the origin of the predictions. Here, we introduce two possible models of the organizational topology of the predictive processing auditory network: (1) the global view, that assumes that predictions on the sensory input are generated at high-order levels of the cerebral cortex and transmitted in a cascade of generative models to the subcortical sensory pathways; and (2) the local view, that assumes that independent local models, computed using local information, are used to perform predictions at each processing stage. In the global view information encoding is optimized globally but biases sensory representations along the entire brain according to the subjective views of the observer. The local view results in a diminished coding efficiency, but guarantees in return a robust encoding of the features of sensory input at each processing stage. Although most experimental results to-date are ambiguous in this respect, recent evidence favors the global model