Altered retrieval of melodic information in congenital amusia: insights from dynamic causal modeling of MEG data

Abstract

Congenital amusia is a neuro-developmental disorder that primarily manifests as a difficulty in the perception and memory of pitch-based materials, including music. Recent findings have shown that the amusic brain exhibits altered functioning of a fronto-temporal network during pitch perception and short-term memory. Within this network, during the encoding of melodies, a decreased right backward frontal-to-temporal connectivity was reported in amusia, along with an abnormal connectivity within and between auditory cortices. The present study investigated whether connectivity patterns between these regions were affected during the short-term memory retrieval of melodies. Amusics and controls had to indicate whether sequences of six tones that were presented in pairs were the same or different. When melodies were different only one tone changed in the second melody. Brain responses to the changed tone in “Different” trials and to its equivalent (original) tone in “Same” trials were compared between groups using Dynamic Causal Modeling (DCM). DCM results confirmed that congenital amusia is characterized by an altered effective connectivity within and between the two auditory cortices during sound processing. Furthermore, right temporal-to-frontal message passing was altered in comparison to controls, with notably an increase in “Same” trials. An additional analysis in control participants emphasized that the detection of an unexpected event in the typically functioning brain is supported by right fronto-temporal connections. The results can be interpreted in a predictive coding framework as reflecting an abnormal prediction error sent by temporal auditory regions towards frontal areas in the amusic brain.

Auditory deficits in amusia extend beyond poor pitch perception

“…Amusia may be congenital (i.e., developed at birth or in early childhood) or can be acquired through brain injury to areas important for music perception (e.g., bilateral damage to superior temporal lobes) (Peretz, 2001; Peretz et al, 1994). Music perception deficits in amusia appear to be linked to an underlying impairment in fine-grained pitch perception (e.g., Foxton et al, 2004; Peretz et al, 2002; Vuvan et al, 2015), either due to deficits in pitch processing (e.g., Cousineau et al, 2015) or deficits in pitch memory (Albouy et al, 2015, 2013a; Gosselin et al, 2009; Tillmann et al, 2016, 2009; Williamson et al, 2010; Williamson and Stewart, 2010). …”

The Neural Causes of Congenital Amusia

“…Alternatively, the pitch-related deficits may be caused by dysfunctions in the frontal cortex (Hyde et al, 2006(Hyde et al, , 2011Albouy et al, 2013). For example, Albouy et al (2013) revealed that low gamma oscillations (30 -40 Hz range) in the right dorsolateral prefrontal cortex (DLPFC) were lower in amusics than in healthy controls. A third possibility, however, is that individuals with congenital amusia have abnormal pitch responsive region(s) in their auditory cortex, despite the fact that the auditory cortex seems to have normal responses to pitch changes (Hyde et al, 2011;Moreauet al, 2013; but see Albouy et al, 2013;Zendel et al, 2015).…”

“…For example, Albouy et al (2013) revealed that low gamma oscillations (30 -40 Hz range) in the right dorsolateral prefrontal cortex (DLPFC) were lower in amusics than in healthy controls. A third possibility, however, is that individuals with congenital amusia have abnormal pitch responsive region(s) in their auditory cortex, despite the fact that the auditory cortex seems to have normal responses to pitch changes (Hyde et al, 2011;Moreauet al, 2013; but see Albouy et al, 2013;Zendel et al, 2015). NormanHaignere et al (2016) examined the third possibility by investigating pitch-specific activation in the auditory cortex.…”

“…Previous studies have suggested three possible neural causes for congenital amusia. One is that congenital amusia is associated with reduced frontotemporal connectivity, which makes it difficult for people with the disorder to consciously access pitch information encoded in their auditory cortex (Loui et al, 2009;Hyde et al, 2011;Albouy et al, 2013Albouy et al, , 2015but see Chen et al, 2015). Alternatively, the pitch-related deficits may be caused by dysfunctions in the frontal cortex (Hyde et al, 2006(Hyde et al, , 2011Albouy et al, 2013).…”

“…One is that congenital amusia is associated with reduced frontotemporal connectivity, which makes it difficult for people with the disorder to consciously access pitch information encoded in their auditory cortex (Loui et al, 2009;Hyde et al, 2011;Albouy et al, 2013Albouy et al, , 2015but see Chen et al, 2015). Alternatively, the pitch-related deficits may be caused by dysfunctions in the frontal cortex (Hyde et al, 2006(Hyde et al, , 2011Albouy et al, 2013). For example, Albouy et al (2013) revealed that low gamma oscillations (30 -40 Hz range) in the right dorsolateral prefrontal cortex (DLPFC) were lower in amusics than in healthy controls.…”