Effect of Auditory Cortex Deactivation on Stimulus-Specific Adaptation in the Medial Geniculate Body

Auditory Neurophysiology Unit, Laboratory for the Neurobiology of Hearing, Institute of Neuroscience of Castilla y León, Calle Pintor Fernando Gallego, 1, Spain.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 11/2011; 31(47):17306-16. DOI: 10.1523/JNEUROSCI.1915-11.2011
Source: PubMed


An animal's survival may depend on detecting new events or objects in its environment, and it is likely that the brain has evolved specific mechanisms to detect such changes. In sensory systems, neurons often exhibit stimulus-specific adaptation (SSA) whereby they adapt to frequently occurring stimuli, but resume firing when "surprised" by rare or new ones. In the auditory system, SSA has been identified in the midbrain, thalamus, and auditory cortex (AC). It has been proposed that the SSA observed subcortically originates in the AC as a higher-order property that is transmitted to the subcortical nuclei via corticofugal pathways. Here we report that SSA in the auditory thalamus of the rat remains intact when the AC is deactivated by cooling, thus demonstrating that the AC is not necessary for the generation of SSA in the thalamus. The AC does, however, modulate the responses of thalamic neurons in a way that strongly indicates a gain modulation mechanism. The changes imposed by the AC in thalamic neurons depend on the level of SSA that they exhibit.

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Available from: Flora M Antunes
    • "In contrast, according to the adaptation hypotheses, the MMN does not reflect a higher level comparison process, but rather represents differences in adaptation of neural elements tuned to the properties of the regular stimuli (the standards) vs. rare stimuli (the deviants) (Jaaskelainen et al., 2004; May & Tiitinen, 2010). Adaptation can be readily observed as stimulus-specific adaptation (SSA) at many levels of the mammalian auditory system including the inferior colliculus (Ayala & Malmierca, 2012; Duque, Perez-Gonzalez, Ayala, Palmer, & Malmierca, 2012; Malmierca, Cristaudo, Perez-Gonzalez, & Covey, 2009; Perez-Gonzalez, Malmierca, & Covey, 2005), the medial geniculate body (Anderson, Christianson, & Linden, 2009; Antunes & Malmierca, 2011), and the auditory cortex (Taaseh, Yaron, & Nelken, 2011; Ulanovsky, Las, Farkas, & Nelken, 2004; Ulanovsky, Las, & Nelken, 2003), and therefore, it has the potential to be a contributing factor in the generation of the MMN, even though the latency of SSA vs. MMN is dramatically different. In humans, MMN is often measured and observed as a component partially overlapping temporally [with small stimulus change, see (Tiitinen, May, Reinikainen, & Näätänen, 1994)], but separate, to the obligatory N1 component that occurs at approximately 100 ms. "
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    ABSTRACT: The mismatch negativity (MMN) component of the auditory event-related potential, elicited in response to unexpected stimuli in the auditory environment, has great value for cognitive neuroscience research. It is changed in several neuropsychiatric disorders such as schizophrenia. The ability to measure and manipulate MMN-like responses in animal models, particularly rodents, would provide an enormous opportunity to learn more about the neurobiology underlying MMN. However, the MMN in humans is a very specific phenomenon: how do we decide which features we should focus on emulating in an animal model to achieve the highest level of translational validity? Here we discuss some of the key features of MMN in humans and summarise the success with which they have been translated into rodent models. Many studies from several different labs have successfully shown that the rat brain is capable of generating deviance detection responses that satisfy of the criteria for the human MMN.
    No preview · Article · Jul 2015 · Biological psychology
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    • "Whether auditory deviance detection in midbrain and thalamic structures emerges from sensorial input proceeding in a feedforward fashion, or it rather results from back-ward information traveling down the cortico-fugal pathway is still a matter of debate (cfr., Escera and Malmierca, 2014). To this regard, recent studies in rodents have demonstrated that reversible deactivation of auditory cortex does not prevent either collicular or thalamic SSA to occur (Antunes and Malmierca, 2011; Anderson and Malmierca, 2013). Additionally, SSA in the IC displays much shorter latencies than that in the auditory cortex (Malmierca et al., 2009). "
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    ABSTRACT: Prompt detection of unexpected changes in the sensory environment is critical for survival. In the auditory domain, the occurrence of a rare stimulus triggers a cascade of neurophysiological events spanning over multiple time-scales. Besides the role of the mismatch negativity (MMN), whose cortical generators are located in supratemporal areas, cumulative evidence suggests that violations of auditory regularities can be detected earlier and lower in the auditory hierarchy. Recent human scalp recordings have shown signatures of auditory mismatch responses at shorter latencies than those of the MMN. Moreover, animal single-unit recordings have demonstrated that rare stimulus changes cause a release from stimulus-specific adaptation in neurons of the primary auditory cortex, the medial geniculate body (MGB), and the inferior colliculus (IC). Although these data suggest that change detection is a pervasive property of the auditory system which may reside upstream cortical sites, direct evidence for the involvement of subcortical stages in the human auditory novelty system is lacking. Using event-related functional magnetic resonance imaging during a frequency oddball paradigm, we here report that auditory deviance detection occurs in the MGB and the IC of healthy human participants. By implementing a random condition controlling for neural refractoriness effects, we show that auditory change detection in these subcortical stations involves the encoding of statistical regularities from the acoustic input. These results provide the first direct evidence of the existence of multiple mismatch detectors nested at different levels along the human ascending auditory pathway.
    Full-text · Article · Feb 2015 · Neuropsychologia
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    • "However, there is now a substantial body of evidence challenging this idea (Pérez-González et al., 2005, 2012; Anderson et al., 2009; Malmierca et al., 2009; Yu et al., 2009; Antunes et al., 2010; Antunes and Malmierca, 2011, 2013; Bäuerle et al., 2011; Zhao et al., 2011; Duque et al., 2012, 2014; Patel et al., 2012; Ayala et al., 2013; Ayala and Malmierca, 2013; Pérez-González and Malmierca, 2014). These studies have demonstrated that SSA also occurs subcortically (Figure 1A), i.e., in the IC and medial geniculate body (MGB). "
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    ABSTRACT: The ability to detect unexpected stimuli in the acoustic environment and determine their behavioral relevance to plan an appropriate reaction is critical for survival. This perspective article brings together several viewpoints and discusses current advances in understanding the mechanisms the auditory system implements to extract relevant information from incoming inputs and to identify unexpected events. This extraordinary sensitivity relies on the capacity to codify acoustic regularities, and is based on encoding properties that are present as early as the auditory midbrain. We review state-of-the-art studies on the processing of stimulus changes using non-invasive methods to record the summed electrical potentials in humans, and those that examine single-neuron responses in animal models. Human data will be based on mismatch negativity (MMN) and enhanced middle latency responses (MLR). Animal data will be based on the activity of single neurons at the cortical and subcortical levels, relating selective responses to novel stimuli to the MMN and to stimulus-specific neural adaptation (SSA). Theoretical models of the neural mechanisms that could create SSA and novelty responses will also be discussed.
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