Mismatch brain response to speech sound changes in rats

Abstract

Understanding speech is based on neural representations of individual speech sounds. In humans, such representations are capable of supporting an automatic and memory-based mechanism for auditory change detection, as reflected by the mismatch negativity (MMN) of event-related potentials. There are also findings of neural representations of speech sounds in animals, but it is not known whether these representations can support the change detection mechanism analogous to that underlying the MMN in humans. To this end, we presented synthesized spoken syllables to urethane-anesthetized rats while local field potentials were epidurally recorded above their primary auditory cortex. In an oddball condition, a deviant stimulus /ga/ or /ba/ (probability 1:12 for each) was rarely and randomly interspersed between frequently presented standard stimulus /da/ (probability 10:12). In an equiprobable condition, 12 syllables, including /da/, /ga/, and /ba/, were presented in a random order (probability 1:12 for each). We found evoked responses of higher amplitude to the deviant /ba/, albeit not to /ga/, relative to the standard /da/ in the oddball condition. Furthermore, the responses to /ba/ were higher in amplitude in the oddball condition than in the equiprobable condition. The findings suggest that anesthetized rat’s brain can form representations of human speech sounds, and that these representations can support the memory-based change detection mechanism analogous to that underlying the MMN in humans. Our findings show a striking parallel in speech processing between humans and rodents and may thus pave the way for feasible animal models of memory-based change detection.

Distinctive Representation of Mispredicted and Unpredicted Prediction Errors in Human Electroencephalography

“…The dissociation conforms to previous research on the MMN reporting a significant "surprise response" by contrasting between a deviant embedded in a standard sequence (i.e., a mispredicted tone) and a deviant embedded in an equiprobable sequence (i.e., an unpredicted tone) (for review, see Jacobsen and Schröger, 2001;Näätänen et al, 2005; but see Ahmed et al, 2011;Astikainen et al, 2011;Nakamura et al, 2011vs Farley et al, 2010Fishman and Steinschneider, 2012;Kaliukhovich and Vogels, 2014 for an ongoing debate in animal research). Importantly, in addition, our results demonstrate how mispredicted and unpredicted responses are related to predicted response, which can help to explain the seemingly contradictory observations of predictionrelated effects in the literature.…”

Criteria for determining whether mismatch responses exist in animal models: Focus on rodents

“…Several laboratories have utilised the many-standards control sequence to demonstrate that rats exhibit human-like MMRs that are independent from adaptation. Adaptation-independent MMRs have been observed in awake, freely moving rats (Harms et al, 2014;Jung et al, 2013;Nakamura et al, 2011;Sivarao et al, 2014) and anesthetised (Ahmed et al, 2011;Astikainen et al, 2011;Nakamura et al, 2011;Shiramatsu et al, 2013) rats, using a variety of different anaesthetic agents (urethane, fentanyl/medetomidine and isoflurane). In addition, deviance detection was identified for a range of stimulus types, including frequency Harms et al, 2014;Jung et al, 2013;Nakamura et al, 2011;Shiramatsu et al, 2013;Sivarao et al, 2014), duration (Nakamura et al, 2011) and speech sounds (Ahmed et al, 2011).…”

“…Adaptation-independent MMRs have been observed in awake, freely moving rats (Harms et al, 2014;Jung et al, 2013;Nakamura et al, 2011;Sivarao et al, 2014) and anesthetised (Ahmed et al, 2011;Astikainen et al, 2011;Nakamura et al, 2011;Shiramatsu et al, 2013) rats, using a variety of different anaesthetic agents (urethane, fentanyl/medetomidine and isoflurane). In addition, deviance detection was identified for a range of stimulus types, including frequency Harms et al, 2014;Jung et al, 2013;Nakamura et al, 2011;Shiramatsu et al, 2013;Sivarao et al, 2014), duration (Nakamura et al, 2011) and speech sounds (Ahmed et al, 2011). Additional studies in anesthetised rats, rather than using a many-standards sequence to control for adaptation, used complex deviations that involve combinations of stimulus features such that each individual feature occurs equally often and therefore subjected to equal amounts of adaptation, such as frequency x intensity conjunctions (Astikainen et al, 2006) or frequency-intensity relationship 'rules' (Astikainen et al, 2014).…”

Auditory cortical and hippocampal local-field potentials to frequency deviant tones in urethane-anesthetized rats: An unexpected role of the sound frequencies themselves

“…It was also not simultaneous with the dentate activity (Ruusuvirta et al, 2013) observed not until in the time window of 125-174.5 ms. Second, differential responses in the auditory cortex unexpectedly appeared to precede those in the dentate gyrus (Ruusuvirta et al, 2013). Third, differential responses in the auditory cortex were not found to be affected by the removal of the standard tone from the series, i.e., by the switch from the oddball condition to the equiprobability condition (Ruusuvirta et al, 1998;Ahmed et al, 2011; for freely moving rats, see, Harms et al, 2015). Fourth, and most importantly, these responses could not even be linked to the rarity of the deviant tones relative to the standard tone but merely to the fact that these tones were of different sound frequencies.…”

“…Deviant tones also elicit differential brain responses (higher-amplitude brain responses to deviant than standard tones) in awake (e.g., Javitt et al, 1994;Ruusuvirta et al, 1995Ruusuvirta et al, , 2010Pincze et al, 2001), sleeping (e.g., Csépe et al, 1987) and anesthetized (e.g., Kraus et al, 1994;Ruusuvirta et al, 1996;Ahmed et al, 2011;Astikainen et al, 2011;Nakamura et al, 2011;Tikhonravov et al, 2008) animals (for negative findings in anesthetized rats see, however, Erikson & Villa, 2005;Lazar & Metherate, 2003). Furthermore, similarly to MMN (Jacobsen and Schröger, 2001), differential brain responses in animals have been attributed to deviant tones as changes in the repetitiveness of a standard tone rather than as rare tones relative to the standard tone (e.g., Ruusuvirta et al, 1998;Nakamura et al, 2011;Taaseh et al, 2011;Jung et al, 2013;Shiramatsu et al, 2013;Harms et al, 2014;Malmierca et al, 2014).…”