The integration of large-scale neural network modeling and functional brain imaging in speech motor control

Abstract

Speech production demands a number of integrated processing stages. The system must encode the speech motor programs that command movement trajectories of the articulators and monitor transient spatiotemporal variations in auditory and somatosensory feedback. Early models of this system proposed that independent neural regions perform specialized speech processes. As technology advanced, neuroimaging data revealed that the dynamic sensorimotor processes of speech require a distributed set of interacting neural regions. The DIVA (Directions into Velocities of Articulators) neurocomputational model elaborates on early theories, integrating existing data and contemporary ideologies, to provide a mechanistic account of acoustic, kinematic, and functional magnetic resonance imaging (fMRI) data on speech acquisition and production. This large-scale neural network model is composed of several interconnected components whose cell activities and synaptic weight strengths are governed by differential equations. Cells in the model are associated with neuroanatomical substrates and have been mapped to locations in Montreal Neurological Institute stereotactic space, providing a means to compare simulated and empirical fMRI data. The DIVA model also provides a computational and neurophysiological framework within which to interpret and organize research on speech acquisition and production in fluent and dysfluent child and adult speakers. The purpose of this review article is to demonstrate how the DIVA model is used to motivate and guide functional imaging studies. We describe how model predictions are evaluated using voxel-based, region-of-interest-based parametric analyses and inter-regional effective connectivity modeling of fMRI data.

Figure 1

Schematic of the DIVA neural network model. Each box corresponds to a set of neurons (or map) and arrows between the boxes correspond to synaptic projections that transform one type of neural representation into another. The model is divided into two basic systems: the Feedforward Control Subsystem on the left and the Feedback Control Subsystem on the right. The neural substrates underlying this integrated control scheme include the premotor and primary motor cortices, somatosensory cortices, auditory cortices, the cerebellum, and the basal ganglia. Matlab source code for the DIVA model and a version of the Maeda (1990) vocal tract that may be used to produce simulated speech output is available at our website (http://speechlab.bu.edu/software.php). Abbreviations: aSMg = anterior supramarginal gyrus; Cau = caudate; Pal = pallidum; Hg = Heschl's gyrus; pIFg = posterior inferior frontal gyrus; pSTg= posterior superior temporal gyrus; PT = planum temporale; Put = Putamen; slCB = superior lateral cerebellum; smCB = superior medial cerebellum; SMA = supplementary motor area; Tha = thalamus; VA = ventral anterior nucleus of the cerebellum; VL = ventral lateral nucleus of the thalamus; vMC = ventral motor cortex; vPMC = ventral premotor cortex; vSC = ventral somatosensory cortex.

Figure 2

Empirical (A) and simulated (B) fMRI data demonstrating the comparable responses for the shift – no shift contrast. Figure is reprinted from Tourville et al. (2008) with permission from the authors.

Figure 3

A cortical and cerebellar parcellation scheme based on the Caviness et al. (1996) parcellation scheme. Dashed lines indicate boundaries between adjacent regions. The intra-Sylvian region is schematized as an exposed flattened surface as indicated by the red arrow. The detached labeled cerebellum is also shown in the lower left and lower right. ROI abbreviations: aCGg = anterior cingulate gyrus; aCO = anterior central operculum; adPMC = anterior dorsal premotor cortex; adSTs = anterior dorsal superior temporal sulcus; Ag = angular gyrus; aIFs = anterior inferior frontal sulcus; aINS = anterior insula; aITg = anterior inferior temporal gyrus; alCB = anterior lateral cerebellum; amCB = anterior medial cerebellum; aMFg = anterior middle frontal gyrus; aMTg = anterior middle temporal gyrus; Amyg = amygdala; aPH = anterior parahippocampal gyrus; aSMg = anterior supramarginal gyrus; aSTg = anterior superior temporal gyrus; aTFg = anterior temporal fusiform gyrus; avSTs = anterior ventral superior temporal sulcus; Caud = caudate; DCN = deep cerebellar nuclei; dIFo = dorsal inferior frontal gyrus, pars opercularis; dIFt = dorsal inferior frontal gyrus, pars triangularis; dMC = dorsal primary motor cortex; dSC = dorsal somatosensory cortex; FMC = frontal medial cortex; FO = frontal operculum; FOC = fronto-orbital cortex; FP = frontal pole; Hg = Heschl's gyrus; Hip = hippocampus; iplCB =inferior posterior lateral cerebellum; ipmCB = inferior posterior medial cerebellum; ITO = inferior temporal occipital gyrus; Lg = lingual gyrus; mdPMC = middle dorsal premotor cortex; MTO = middle temporal occipital gyrus; OC = occipital cortex; Pal = pallidum; pCGg = posterior cingulate gyrus; pCO = posterior central operculum; PCN = precuneus cortex; pdPMC = posterior dorsal premotor cortex; pdSTs = posterior dorsal superior temporal sulcus; PHg = parahippocampal gyrus; pIFs = posterior inferior frontal sulcus; pINS = posterior insula; pITg = posterior inferior temporal gyrus; pMFg = posterior middle frontal gyrus; pMTg = posterior middle temporal gyrus; PO = parietal operculum; PP = planum polare; pPH = posterior parahippocampal gyrus; preSMA = pre-supplementary motor area; pSMg = posterior supramarginal gyrus; pSTg = posterior superior temporal gyrus; PT = planum temporale; pTFg = posterior temporal fusiform gyrus; pvSTs = posterior ventral superior temporal sulcus; Put = putamen; SCC = subcallosal cortex; SFg = superior frontral gyrus; slCB = superior lateral cerebellum; SMA = supplementary motor area; smCB = superior medial cerebellum; SPL = superior parietal lobule; splCB = superior posterior lateral cerebellum; spmCB = superior posterior medial cerebellum; Tha = thalamus; TOF = temporal occipital fusiform gyrus; TP = temporal pole; vIFo = ventral inferior frontal gyrus, pars opercularis; vIFt = ventral inferior frontal gyrus, pars triangularis; vMC = ventral primary motor cortex; vPMC = ventral premotor cortex; vSC = ventral somatosensory cortex. Sulci abbreviations: aasf = anterior association ramus of the Sylvian fissure; ahsf = anterior horizontal ramus of the Sylvian fissure; ccs = calcarine sulcus; cgs = cingulate sulcus; cis = central insular sulcus; cs = central sulcus; cos = collateral sulcus; crs = circular sulcus; ftts = first transverse temporal sulcus; hfcb = horizontal fissure of the cerebellum; hs = Heschl's sulcus; ifrs = inferior frontal sulcus; itps = itraparietal sulcus; its = inferior temporal sulcus; locs = lateral occipital sulcus; ots = occipitotemporal sulcus; pasf = posterior ascending Sylvian fissure; pfcb = primary fissure of the cerebellum; pis = primary intermediate sulcus; pocs = postcentral sulcus; pos = parieto-occipital sulcus; prcs = precentral sulcus; sbps = subparietal sulcus; sf = Sylvian fissure; sfrs = superior frontal sulcus; sts = superior temporal sulcus

Figure 4

Neuroanatomical mapping of the DIVA model. A. The location of DIVA model component sites (red dots) are plotted on a schematic of the left hemisphere. Medial regions are shown on the left, lateral regions on the right. B. A schematic of the right hemisphere lateral Rolandic and inferior frontal region. The corresponding contralateral region in the left hemisphere is outlined by the dashed box in A. The right hemisphere plot demonstrates the location of the Feedback Control Map and the location of motor and somatosensory representations of the articulators. Abbreviations: ΔAu = auditory error map; ΔS = somatosensory error map; Au = auditory state map; CBM_DCN = deep cerebellar nuclei; CBM_Lat = lateral cerebellum; CBM_Med = medial cerebellum; FB = feedback control map; IM_Cau = caudate initiation map; IM_SMA = supplementary motor area initiation map; IM_Tha = thalamus initiation map; IM_Pal, = pallidum initiation map; IM_Put = putamen initiation map; Larynx_Int = intrinsic larynx; Larynx_Ext = extrinsic larynx; M = articulator position map; Ṁ = articulator velocity map; Resp = respiratory motor cells; S = somatosensory state map; SSM = speech sound map; T_Au = auditory target map; T_S = somatosensory target map.

Figure 5

The difference between the normalized effects of the right and left hemispheres are shown for four ROIs that were found to differ significantly in at least one contrast (no shift – baseline, shift – baseline, shift – no shift). Positive difference values indicate a greater effect in the right hemisphere. The p-value is provided in red for those tests that resulted in a significant laterality effect. The laterality tests demonstrated left lateralized effects in the ventral frontal ROIs in the no shift – baseline contrast; this lateralized effect shifted to the right hemisphere in the shift – no shift contrast in ventral premotor cortex. Abbreviations: amCB = anterior medial cerebellum; IFo = inferior frontal gyrus, pars opercularis; vPMC = ventral premotor cortex; vMC = ventral motor cortex.

Figure 6

Schematic of the path diagram evaluated by structural equation modeling. Effective connectivity within the network of regions shown was significantly modulated by the auditory feedback perturbation. Path coefficients for all projections shown were significant in both conditions except that from right vMC to right vPMC (no shift condition p = 0.07). Pair-wise comparisons of path coefficients in the two conditions revealed significant interactions (highlighted in bold) due to the shift in auditory feedback in the projections between left pSTg to right pSTg, from left pSTg to right vPMC, and from right pSTg to right IFt. Abbreviations: IFt = inferior frontal gyrus, pars triangularis; pSTg = posterior superior temporal gyrus; vMC = ventral motor cortex; vPMC = ventral premotor cortex.

Figure 7

Schematic highlighting the right-lateralized Feedback Control Map and associated projections (indicated in bold). Abbreviations: Hg = Heschl's gyrus; pIFg = posterior inferior frontal gyrus; pSTg = posterior superior temporal gyrus; PT = planum temporale; slCB = superior lateral cerebellum; smCB = superior medial cerebellum; VA = ventral anterior nucleus of the thalamus; VL = ventral lateral nucleus of the thalamus; vMC = ventral motor cortex; vPMC = ventral premotor cortex.