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Spontaneous low threshold spike bursting in awake humans is different in different lateral thalamic nuclei

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Abstract

Spontaneous action potential bursts associated with low threshold calcium spikes (LTS) occur in multiple human lateral thalamic nuclei, each with different physiologic characteristics. We now test the hypothesis that different patterns of spontaneous LTS bursting occur in these nuclei during awake surgery in patients with essential tremor and the arm at rest. This protocol was chosen to minimize the effect of the patient’s disease upon thalamic activity which is a potential confound in a surgical study of this type. Neuronal activity was studied in the human thalamic nuclei receiving somatic sensory input (Vc, ventral caudal), input from the deep cerebellar nuclei (Vim, ventral intermediate), or input from the pallidum (Vo, ventral oral). In each nucleus the burst rates were significantly greater than zero. Burst rates were higher in Vc than in Vim, while firing rates were lower. These findings suggest that neurons in Vc are hyperpolarized and have more frequent inhibitory events. Pre-burst inter-spike intervals (ISIs) were significantly longer in Vc, but were significantly shorter when corrected for the average ISIs between bursts (burst rate/inverse of the primary event rate). These results suggest that inhibitory events in Vc are of lower magnitude relative to a hyperpolarized resting membrane potential. Studies in many species demonstrate that input from the pallidum to the thalamus is inhibitory, suggesting that input to Vo is predominantly inhibitory. However, neurons in Vo have neither slower firing rates nor more frequent LTS bursts. Previous studies have found that spontaneous LTS is similar between classes of neurons within Vc, as defined by their response to thermal and painful stimuli. The differences in spontaneous LTS between human nuclei but not between functional classes within a nucleus may be a basic organizing principle of thalamic inhibitory circuitry.

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References

  • Anderson ME, Turner DM (1991) Activity of neurons in cerebellar-receiving and pallidal-receiving areas of the thalamus of the behaving monkey. J Neurophysiol 66:879–893

    PubMed  CAS  Google Scholar 

  • Apkarian AV, Hodge CJ (1989) Primate spinothalamic pathways: III. Thalamic terminations of the dorsolateral and ventral spinothalamic pathways. J Comp Neurol 288:493–511

    Article  PubMed  CAS  Google Scholar 

  • Cox DR, Lewis PAW (1966) The statistical analysis of series of events. Chapman and Hall, London

    Google Scholar 

  • DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–285

    Article  PubMed  CAS  Google Scholar 

  • Deuschl G, Bain P, Brin M (1998) Consensus statement of the Movement Disorder Society on Tremor. Ad Hoc Scientific Committee. Mov Disord 13(Suppl 3):2–23

    Google Scholar 

  • Deuschl G, Krack P, Lauk M, Timmer J (1996) Clinical neurophysiology of tremor. J Clin Neurophysiol 13:110–121

    Article  PubMed  CAS  Google Scholar 

  • Elble RJ (2002) Essential tremor is a monosymptomatic disorder. Mov Disord 17:633–637

    Article  PubMed  Google Scholar 

  • Elble RJ, Koller W (1990) Tremor. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Garonzik IM, Hua SE, Ohara S, Lenz FA (2002) Intraoperative microelectrode and semi-microelectrode recording during the physiological localization of the thalamic nucleus ventral intermediate. Mov Disord 17(Suppl 3):S135–S144

    Article  PubMed  Google Scholar 

  • Hirai T, Jones EG (1989) A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Rev 14:1–34

    Article  PubMed  CAS  Google Scholar 

  • Hua SE, Lenz FA (2005) Posture-related oscillations in human cerebellar thalamus in essential tremor are enabled by voluntary motor circuits. J Neurophysiol 93:117–127

    Article  PubMed  Google Scholar 

  • Hua SE, Lenz FA, Zirh TA, Reich SG, Dougherty PM (1998) Thalamic neuronal activity correlated with essential tremor. J Neurol Neurosurg Psychiatr 64:273–276

    Article  PubMed  CAS  Google Scholar 

  • Jahnsen H, Llinas R (1984a) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol 349:205–226

    CAS  Google Scholar 

  • Jahnsen H, Llinas R (1984b) Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349:227–247

    CAS  Google Scholar 

  • Jankovic J (2002) Essential tremor: a heterogenous disorder. Mov Disord 17:638–644

    Article  PubMed  Google Scholar 

  • Jeanmonod D, Magnin M, Morel A (1996) Low-threshold calcium spike bursts in the human thalamus. Common physiopathology for sensory, motor and limbic positive symptoms. Brain 119(Pt 2):363–375

    Article  PubMed  Google Scholar 

  • Jenkins IH, Bain PB, Colebatch JG, Thompson PD, Findley LJ, Frackowiak RSJ, Marsden CD, Brooks DJ (1993) A positron emission tomography study of essential tremor: evidence of overactivity of cerebellar connections. Ann Neurol 34:82–90

    Article  PubMed  CAS  Google Scholar 

  • Koller WC, Lyons KE, Wilkinson SB, Troster AI, Pahwa R (2001) Long-term safety and efficacy of unilateral deep brain stimulation of the thalamus in essential tremor. Mov Disord 16:464–468

    Article  PubMed  CAS  Google Scholar 

  • Lee JI, Ohara S, Dougherty PM, Lenz FA (2005) Pain and temperature encoding in the human thalamic somatic sensory nucleus (ventral caudal): inhibition-related bursting evoked by somatic stimuli. J Neurophysiol 94:1676–1687

    Article  PubMed  Google Scholar 

  • Lenz FA, Dougherty PM (1998) Cells in the human principal thalamic sensory nucleus (ventralis caudalis—Vc) respond to innocuous mechanical and cool stimuli. J Neurophysiol 79:2227–2230

    PubMed  CAS  Google Scholar 

  • Lenz FA, Kwan HC, Dostrovsky JO, Tasker RR (1989) Characteristics of the bursting pattern of action potentials that occurs in the thalamus of patients with central pain. Brain Res 496:357–360

    Article  PubMed  CAS  Google Scholar 

  • Lenz FA, Kwan HC, Martin R, Tasker R, Richardson RT, Dostrovsky JO (1994) Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection. J Neurophysiol 72:1570–1587

    PubMed  CAS  Google Scholar 

  • Lenz FA, Normand SL, Kwan HC, Andrews D, Rowland LH, Jones MW, Seike M, Lin YC, Tasker RR, Dostrovsky JO (1995) Statistical prediction of the optimal site for thalamotomy in parkinsonian tremor. Mov Disord 10:318–328

    Article  PubMed  CAS  Google Scholar 

  • Lenz FA, Garonzik IM, Zirh TA, Dougherty PM (1998) Neuronal activity in the region of the thalamic principal sensory nucleus (ventralis caudalis) in patients with pain following amputations. Neurosci 86:1065–1081

    Article  CAS  Google Scholar 

  • Lenz FA, Jaeger CJ, Seike MS, Lin YC, Reich SG (2002) Single-neuron analysis of human thalamus in patients with intention tremor and other clinical signs of cerebellar disease. J Neurophysiol 87:2084–2094

    PubMed  CAS  Google Scholar 

  • McCarley RW, Benoit O, Barrionuevo G (1983) Lateral geniculate nucleus unitary discharge in sleep and waking: state and rate specific aspects. J Neurophysiol 50:798–818

    PubMed  CAS  Google Scholar 

  • Molnar GF, Pilliar A, Lozano AM, Dostrovsky JO (2005) Differences in neuronal firing rates in pallidal and cerebellar receiving areas of thalamus in patients with Parkinson’s disease, essential tremor, and pain. J Neurophysiol 93:3094–3101

    Article  PubMed  CAS  Google Scholar 

  • Ohara S, Lenz FA (2003) Medial lateral extent of thermal and pain sensations evoked by microstimulation in somatic sensory nuclei of human thalamus. J Neurophysiol 90:2367–2377

    Article  PubMed  Google Scholar 

  • Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83:117–161

    PubMed  CAS  Google Scholar 

  • Radhakrishnan V, Tsoukatos J, Davis KD, Tasker RR, Lozano AM, Dostrovsky JO (1999) A comparison of the burst activity of lateral thalamic neurons in chronic pain and non-pain patients. Pain 80:567–575

    Article  PubMed  CAS  Google Scholar 

  • Ramcharan EJ, Cox CL, Zhan XJ, Sherman SM, Gnadt JW (2000a) Cellular mechanisms underlying activity patterns in the monkey thalamus during visual behavior. J Neurophysiol 84:1982–1987

    CAS  Google Scholar 

  • Ramcharan EJ, Gnadt JW, Sherman SM (2000b) Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis Neurosci 17:55–62

    Article  CAS  Google Scholar 

  • Schaltenbrand G, Bailey P (1959) Introduction to stereotaxis with an atlas of the human brain. Thiem, Stuttgart

    Google Scholar 

  • Sherman SM, Guillery RW (2001) Exploring the thalamus and its role in cortical function. Oxford University Press, New York

    Google Scholar 

  • Smith GD, Sherman SM (2002) Detectability of excitatory versus inhibitory drive in an integrate-and-fire-or-burst thalamocortical relay neuron model. J Neurosci 22:10242–10250

    PubMed  CAS  Google Scholar 

  • Steriade M, Jones EG, Llinas RR (1990) Thalamic oscillations and signaling. Wiley, New York

    Google Scholar 

  • Steriade M, Jones EG, McCormick DA (1997) Thalamus organisation and function, vol 1. Elsevier, Amsterdam

  • Zirh AT, Lenz FA, Reich SG, Dougherty PM (1997) Patterns of bursting occurring in thalamic cells during parkinsonian tremor. Neurosci 83:107–121

    Article  Google Scholar 

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Acknowledgments

This study was supported by grants to FAL from the Eli Lilly Corporation and the NIH (NS 383493, NS 40059). We thank L. Rowland for technical assistance.

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Correspondence to F. A. Lenz.

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Ohara, S., Taghva, A., Kim, J.H. et al. Spontaneous low threshold spike bursting in awake humans is different in different lateral thalamic nuclei. Exp Brain Res 180, 281–288 (2007). https://doi.org/10.1007/s00221-007-0856-9

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  • DOI: https://doi.org/10.1007/s00221-007-0856-9

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