Disentangling the influences of multiple thalamic nuclei on prefrontal cortex and cognitive control

Phillips, Jessica M.; Kambi, Niranjan A.; Redinbaugh, Michelle J.; Mohanta, Sounak; Saalmann, Yuri B.

doi:10.1016/j.neubiorev.2021.06.042

Cited by 37 publications

(47 citation statements)

References 327 publications

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“…BOLD signal elevations in the thalamus and reticular formation are consistent with focused attention. Whereas the thalamus, and most especially the reticular thalamus supports selective attention, especially to sensory information (Guillery et al, 1998;Phillips et al, 2021), the reticular formation is critically involved in directing cortical arousal and attention to salient stimuli (Jones, 2003). The detection of the activation of these structures during melodic acoustic stimulation supports that our gradual habituation strategy to awake fMRI supports the discrimination of cognitive processes in the absence of stress confounds.…”

Section: Discussionsupporting

confidence: 51%

Gradual Restraint Habituation for Awake Functional Magnetic Resonance Imaging Combined With a Sparse Imaging Paradigm Reduces Motion Artifacts and Stress Levels in Rodents

et al. 2021

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Functional magnetic resonance imaging, as a non-invasive technique, offers unique opportunities to assess brain function and connectivity under a broad range of applications, ranging from passive sensory stimulation to high-level cognitive abilities, in awake animals. This approach is confounded, however, by the fact that physical restraint and loud unpredictable acoustic noise must inevitably accompany fMRI recordings. These factors induce marked stress in rodents, and stress-related elevations of corticosterone levels are known to alter information processing and cognition in the rodent. Here, we propose a habituation strategy that spans specific stages of adaptation to restraint, MRI noise, and confinement stress in awake rats and circumvents the need for surgical head restraint. This habituation protocol results in stress levels during awake fMRI that do not differ from pre-handling levels and enables stable image acquisition with very low motion artifacts. For this, rats were gradually trained over a period of three weeks and eighteen training sessions. Stress levels were assessed by analysis of fecal corticosterone metabolite levels and breathing rates. We observed significant drops in stress levels to below pre-handling levels at the end of the habituation procedure. During fMRI in awake rats, after the conclusion of habituation and using a non-invasive head-fixation device, breathing was stable and head motion artifacts were minimal. A task-based fMRI experiment, using acoustic stimulation, conducted 2 days after the end of habituation, resulted in precise whole brain mapping of BOLD signals in the brain, with clear delineation of the expected auditory-related structures. The active discrimination by the animals of the acoustic stimuli from the backdrop of scanner noise was corroborated by significant increases in BOLD signals in the thalamus and reticular formation. Taken together, these data show that effective habituation to awake fMRI can be achieved by gradual and incremental acclimatization to the experimental conditions. Subsequent BOLD recordings, even during superimposed acoustic stimulation, reflect low stress-levels, low motion and a corresponding high-quality image acquisition. Furthermore, BOLD signals obtained during fMRI indicate that effective habituation facilitates selective attention to sensory stimuli that can in turn support the discrimination of cognitive processes in the absence of stress confounds.

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Section: Discussionsupporting

confidence: 51%

Gradual Restraint Habituation for Awake Functional Magnetic Resonance Imaging Combined With a Sparse Imaging Paradigm Reduces Motion Artifacts and Stress Levels in Rodents

et al. 2021

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“…Notably, direct comparison using Bayesian contrast revealed a very strong evidence (posterior probability >99%) for increased modulatory connectivity from rIFG to rCau and rThal in the NoGo condition compared to the Go condition, suggesting the rIFG driven engagement of cortical-to-subcortical top-down control during response inhibition. Previous animal models and human neuroimaging meta-analyses have consistently identified the rIFG, as a key region implicated in dopaminergic and noradrenergic modulated inhibitory regulation (Bari et al, 2011; Hauber, 2010; Ott and Nieder, 2019; Pfeifer et al, 2022; Terra et al, 2020; Vijayraghavan et al, 2016; Zhukovsky et al, 2021) in particular during motor control and inhibition (Aron et al, 2003; Chamberlain and Sahakian, 2007; Puiu et al, 2020; Xu et al, 2016), while both, fronto-striatal and fronto-thalamic projections have been extensively involved in response inhibition (Ahissar and Oram, 2015; Bosch-Bouju et al, 2013; Marzinzik et al, 2008; Phillips et al, 2021; Schmitt et al, 2017; Sommer, 2003; Tanaka and Kunimatsu, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…Enhanced norepinephrine signaling facilitates response inhibition via modulation of the IFG and its connections with the striatum (Chamberlain et al, 2009; Rae et al, 2016), while the dorsal striatum represents an important locus of dopaminergic control of response inhibition (Ghahremani et al, 2012; Robertson et al, 2015) and the IFG plays an important role in top-down control of the basal ganglia regions (Buschman and Miller, 2014; Hampshire et al, 2010; Jahfari et al, 2012; Kim, 2014; Puiu et al, 2020; Renteria et al, 2018; Schaum et al, 2020; Tops and Boksem, 2011). In the basal ganglia-thalamocortical model of response inhibition (Alexander et al, 1986, 1991; Alexander and Crutcher, 1990) the thalamus relays information between the basal ganglia and cortex (Collins et al, 2018; Haber and Mcfarland, 2001; Haber and Calzavara, 2009; McFarland and Haber, 2002) - thus facilitating response inhibition and performance monitoring (Bosch-Bouju et al, 2013; Huang et al, 2018; Saalmann and Kastner, 2015; Tanaka and Kunimatsu, 2011) - via dense reciprocal connections with the basal ganglia and PFC (Guillery, 1995; Phillips et al, 2021; Xiao et al, 2009; Tanaka and Kunimatsu, 2011).…”

Section: Introductionmentioning

confidence: 99%

The right inferior frontal gyrus as pivotal node and effective regulator of the basal ganglia-thalamocortical response inhibition circuit

Zhuang

Qiao

Lei

et al. 2022

Preprint

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The involvement of specific basal ganglia-thalamocortical circuits in response inhibition has been extensively mapped in animal models. However, the pivotal nodes and directed casual regulation within this inhibitory circuit in humans remains controversial. Here, we capitalize on the recent progress in robust and biologically plausible directed causal modelling (DCM-PEB) and a large response inhibition dataset (n=218; 104 males) acquired with concomitant functional fMRI to determine key nodes, their causal regulation and modulation via biological variables (sex) and inhibitory performance in the inhibitory circuit encompassing the right inferior frontal gyrus (rIFG), caudate nucleus (rCau), globus pallidum (rGP) and thalamus (rThal). The entire neural circuit exhibited high intrinsic connectivity and response inhibition critically increased causal projections from the rIFG to both rCau and rThal. Direct comparison further demonstrated that response inhibition induced an increasing rIFG inflow and increased the causal regulation of this region over the rCau and rThal. In addition, sex and performance influenced the architecture of the regulatory circuits such that women displayed increased rThal self-inhibition and decreased rThal to GP modulation, while better inhibitory performance was associated with stronger rThal to rIFG communication. Furthermore, control analyses did not reveal a similar key communication in a left lateralized model. Together these findings indicate a pivotal role of the rIFG as input and causal regulator of subcortical response inhibition nodes.

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“…Recent studies have elucidated a role for MD regulating signal processing properties of mPFC neurons and stressed its importance for rapid trial-by-trial learning and complex decision making ( Mitchell and Chakraborty, 2013 ; Mitchell, 2015 ; Mukherjee et al, 2021 ; see above). The rostral intralaminar nuclei are organized to control cortico-cortical and corticostriatal interactions ( Groenewegen and Berendse, 1994 ; Saalmann, 2014 ; Phillips et al, 2021 ). Lesions of these nuclei have more widespread effects on behavior than MD lesions, more closely resembling effects of mPFC and striatal lesions ( Mair et al, 2021 ; Figures 4 – 6 ; see above).…”

Section: Multiple Neural Network Interact To Support Adaptive Goal-di...mentioning

confidence: 99%

Where Actions Meet Outcomes: Medial Prefrontal Cortex, Central Thalamus, and the Basal Ganglia

Mair

Francoeur

Krell

et al. 2022

Front. Behav. Neurosci.

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Medial prefrontal cortex (mPFC) interacts with distributed networks that give rise to goal-directed behavior through afferent and efferent connections with multiple thalamic nuclei and recurrent basal ganglia-thalamocortical circuits. Recent studies have revealed individual roles for different thalamic nuclei: mediodorsal (MD) regulation of signaling properties in mPFC neurons, intralaminar control of cortico-basal ganglia networks, ventral medial facilitation of integrative motor function, and hippocampal functions supported by ventral midline and anterior nuclei. Large scale mapping studies have identified functionally distinct cortico-basal ganglia-thalamocortical subnetworks that provide a structural basis for understanding information processing and functional heterogeneity within the basal ganglia. Behavioral analyses comparing functional deficits produced by lesions or inactivation of specific thalamic nuclei or subregions of mPFC or the basal ganglia have elucidated the interdependent roles of these areas in adaptive goal-directed behavior. Electrophysiological recordings of mPFC neurons in rats performing delayed non-matching-to position (DNMTP) and other complex decision making tasks have revealed populations of neurons with activity related to actions and outcomes that underlie these behaviors. These include responses related to motor preparation, instrumental actions, movement, anticipation and delivery of action outcomes, memory delay, and spatial context. Comparison of results for mPFC, MD, and ventral pallidum (VP) suggest critical roles for mPFC in prospective processes that precede actions, MD for reinforcing task-relevant responses in mPFC, and VP for providing feedback about action outcomes. Synthesis of electrophysiological and behavioral results indicates that different networks connecting mPFC with thalamus and the basal ganglia are organized to support distinct functions that allow organisms to act efficiently to obtain intended outcomes.

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Disentangling the influences of multiple thalamic nuclei on prefrontal cortex and cognitive control

Cited by 37 publications

References 327 publications

Gradual Restraint Habituation for Awake Functional Magnetic Resonance Imaging Combined With a Sparse Imaging Paradigm Reduces Motion Artifacts and Stress Levels in Rodents

Gradual Restraint Habituation for Awake Functional Magnetic Resonance Imaging Combined With a Sparse Imaging Paradigm Reduces Motion Artifacts and Stress Levels in Rodents

The right inferior frontal gyrus as pivotal node and effective regulator of the basal ganglia-thalamocortical response inhibition circuit

Where Actions Meet Outcomes: Medial Prefrontal Cortex, Central Thalamus, and the Basal Ganglia

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