Dual-stream cortical pathways mediate sensory prediction

Abstract

Predictions are constantly generated from diverse sources to optimize cognitive functions in the ever-changing environment. However, the neural origin and generation process of top-down induced prediction remain elusive. We hypothesized that motor-based and memory-based predictions are mediated by distinct descending networks from motor and memory systems to the sensory cortices. Using functional magnetic resonance imaging (fMRI) and a dual imagery paradigm, we found that motor and memory upstream systems activated the auditory cortex in a content-specific manner. Moreover, the inferior and posterior parts of the parietal lobe differentially relayed predictive signals in motor-to-sensory and memory-to-sensory networks. Dynamic causal modeling of directed connectivity revealed selective enabling and modulation of connections that mediate top-down sensory prediction and ground the distinctive neurocognitive basis of predictive processing.

Distinct neural mechanisms support inner speaking and inner hearing

“…This result suggests that the motor simulation stream may also be solicited during inner hearing, but to a lesser extent than during inner speaking (consistent with the results obtained by Tian et al, 2016). 4 By contrasting inner speaking and inner hearing of non-speech sounds, Chu et al (2023) recently showed a clear dissociation in the involvement of the motor-based and memory-based networks, further supporting the distinction between these two processes. Overall, our results are also compatible with the framework recently provided by Pratts et al (2023), in which inner speech can be generated by two separate mechanisms similar to those postulated by the dual stream prediction model, according to the intentionality and egocentricity constraints of the task.…”

RDoC Framework Through the Lens of Predictive Processing: Focusing on Cognitive System Domain

“…Furthermore, human fMRI studies based on the mental imagery paradigm also investigate the PP mechanism within cortico-cortical interactions associated with declarative memory (Chu et al, 2023;Ortiz-Tudela et al, 2023). These studies support the differentiated mechanism between memory and motor-based predictions (Chu et al, 2023), and episodic and semantic predictions (Ortiz-Tudela et al, 2023).…”

“…Meanwhile, in episodic recall descending neurons from the hippocampus can be routed via a disinhibitory pathway, which helps facilitate selective neocortical reinstatement that supports memory recall (Barron et al, 2020). Furthermore, human fMRI studies based on the mental imagery paradigm also investigate the PP mechanism within cortico-cortical interactions associated with declarative memory (Chu et al, 2023;Ortiz-Tudela et al, 2023). These studies support the differentiated mechanism between memory and motor-based predictions (Chu et al, 2023), and episodic and semantic predictions (Ortiz-Tudela et al, 2023).…”

Impaired motor-to-sensory transformation mediates auditory hallucinations

“…Our model, based on two distinct modulatory functions in the motor-to-sensory transformation, assumes two types of predictions that can presumably integrate both inference models. EC serves as a content prediction, resembling the strong priors that would elicit the specific auditory neural representation without corresponding external stimulation [4,8,35,36]. Whereas, CD serves as a prediction for agency, and the impairment would cause the failure to explain away the internally generated auditory neural representations that are evoked by EC [49,52,69,70].…”

“…For example, action-induced enhancement has been found in a subset of sensory cortices in addition to action-induced suppression [30][31][32][33][34]. Auditory neural representations are constructed in auditory working memory based on covert speaking [8,35,36]. This motor-based auditory working memory (i.e.…”