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Crammond, D. J.

Publications and source records attributed to Crammond, D. J..

4 recordsLinked to original sources

Subthalamic nucleus neurons encode syllable sequence and phonetic characteristics during speech

Speech is a complex behavior that can be used to study unique contributions of the basal ganglia to motor control in the human brain. Computational models suggest that the basal ganglia encodes either the phonetic content or the sequence of speech elements. To explore this question, we investigated the relationship between phoneme and sequence features of a spoken syllable triplet and the firing rate of subthalamic nucleus (STN) neurons recorded during the implantation of deep brain stimulation (DBS) electrodes in individuals with Parkinsons disease. Patients repeated aloud a random sequence of three consonant-vowel (CV) syllables in response to audio cues. Single-unit extracellular potentials were sampled from the sensorimotor STN; a total of 227 unit recordings were obtained from the left STN of 25 subjects (4 female). Of these, 113 (50%) units showed significant task-related increased firing and 53 (23%) showed decreased firing (t-test relative to inter-trial period baseline, p<0.05). Linear regression analysis revealed that both populations of STN neurons encode phoneme and sequence features of produced speech. Maximal phoneme encoding occurred at the time of phoneme production, suggesting efference copyor sensory-related processing, rather than speech motor planning (-50ms and +175ms relative to CV transition for consonant and vowel encoding, respectively). These findings demonstrate that involvement of the basal ganglia in speaking includes separate single unit representations of speech sequencing and phoneme selection in the STN.

neuroscience↗

Hyperdirect connectivity of opercular speech network to the subthalamic nucleus

The importance of the basal ganglia in modulating cognitive and motor behaviors is well known, yet how the basal ganglia participate in the uniquely human behavior of speech is poorly understood. The subthalamic nucleus (STN) is well positioned to facilitate two basal ganglia functions critical for speech: motor learning and gain modulation. Using a novel paradigm to study cortical-subcortical interactions during speech in patients undergoing awake DBS surgery, we found evidence for a left opercular hyperdirect pathway in humans by stimulating in the STN and examining antidromic evoked activity in the left temporal, parietal and frontal opercular cortex. These high resolution cortical and subcortical mapping data provided evidence for hyperdirect connectivity between Brocas area (typically corresponding to pars triangularis and pars opercularis of the inferior frontal gyrus) and the STN. In addition, we observed evoked potentials consistent with the presence of monosynaptic projections from areas of opercular speech cortex that are primarily sensory, including auditory cortex, to the STN. These connections may be unique to humans, evolving alongside the ability for speech. SIGNIFICANCEUsing intracranial recordings from the basal ganglia and cortex in subjects undergoing deep brain stimulation, this study provides evidence for monosynaptic cortical inputs from motor planning, motor sensory, and auditory sensory cortices to the subthalamic nucleus. These observations suggest that in humans, the cortical-basal ganglia hyperdirect pathway is uniquely positioned to participate in speech production. Moreover, the existence of a monosynaptic connection between human sensory cortical areas and the subthalamic nucleus indicates a need to update traditional models of information transfer within cortical-basal ganglia-thalamocortical circuitry, which has significant implications for understanding other human cognitive behavior or dysfunction.

neuroscience↗

Subthalamic nucleus and sensorimotor cortex activity during speech production

The sensorimotor cortex is somatotopically organized to represent the vocal tract articulators, such as lips, tongue, larynx, and jaw. How speech and articulatory features are encoded at the subcortical level, however, remains largely unknown. We analyzed local field potential (LFP) recordings from the subthalamic nucleus (STN) and simultaneous electrocorticography recordings from the sensorimotor cortex of 11 patients (1 female) with Parkinsons disease during implantation of deep brain stimulation (DBS) electrodes, while patients read aloud three-phoneme words. The initial phonemes involved either articulation primarily with the tongue (coronal consonants) or the lips (labial consonants). We observed significant increases in high gamma (60-150 Hz) power in both the STN and the sensorimotor cortex that began before speech onset and persisted for the duration of speech articulation. As expected from previous reports, in the sensorimotor cortex, the primary articulator involved in the production of the initial consonant was topographically represented by high gamma activity. We found that STN high gamma activity also demonstrated specificity for the primary articulator, although no clear topography was observed. In general, subthalamic high gamma activity varied along the ventral-dorsal trajectory of the electrodes, with greater high gamma power recorded in the more dorsal locations of the STN. These results demonstrate that articulator-specific speech information is contained within high gamma activity of the STN, with similar temporal but less specific topographical organization, compared to similar information encoded in the sensorimotor cortex.\n\nSIGNIFICANCE STATEMENTClinical and electrophysiological evidence suggests that the subthalamic nucleus is involved in speech, however, this important basal ganglia node is ignored in current models of speech production. We previously showed that subthalamic nucleus neurons differentially encode early and late aspects of speech production, but no previous studies have examined subthalamic functional organization for speech articulators. Using simultaneous local field potential recordings from the sensorimotor cortex and the subthalamic nucleus in patients with Parkinsons disease undergoing deep brain stimulation surgery, we discovered that subthalamic nucleus high gamma activity tracks speech production at the level of vocal tract articulators, with high gamma power beginning to increase prior to the onset of vocalization, similar to cortical articulatory encoding.

neuroscience↗

Subthalamic nucleus neurons differentially encode early and late aspects of speech production

Basal ganglia-thalamocortical loops mediate all motor behavior, yet little detail is known about the role of basal ganglia nuclei in speech production. Using intracranial recording during deep brain stimulation surgery, we tested the hypothesis that the firing rate of subthalamic nucleus neurons is modulated in response to both planning and motor execution aspects of speech. Nearly half of 79 recorded units exhibited firing rate modulation, during a syllable reading task administered in 12 subjects. Trial-to-trial timing of changes in subthalamic neuronal activity, relative to cue onset versus production onset, revealed that locking to cue presentation was associated more with units that decreased firing rate, while locking to speech onset was associated more with units that increased firing rate. These uniquely acquired data indicate that subthalamic activity is dynamic during the production of speech, reflecting temporally-dependent inhibition and excitation of separate populations of subthalamic neurons.

neuroscience↗