Cortically induced thalamic plasticity in the primate somatosensory system

Ergenzinger, Edward R; Glasier, Marylou M.; Hahm, Jong-On; Pons, T. P.

doi:10.1038/673

Cited by 149 publications

(81 citation statements)

References 22 publications

(27 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…A treatment of the SI for several months with an NMDA receptor agonist induces a large change in the somatotopic map in the thalamus (32). This intriguing finding most likely indicates that the corticofugal system can modulate the subcortical somatotopic map.…”

Section: Discussionmentioning

confidence: 81%

Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system

Gao

Suga²

1998

Proc. Natl. Acad. Sci. U.S.A.

204

137

View full text Add to dashboard Cite

Recent studies of corticofugal modulation of auditory information processing indicate that cortical neurons mediate both a highly focused positive feedback to subcortical neurons ''matched'' in tuning to a particular acoustic parameter and a widespread lateral inhibition to ''unmatched'' subcortical neurons. This cortical function for the adjustment and improvement of subcortical information processing is called egocentric selection. Egocentric selection enhances the neural representation of frequently occurring signals in the central auditory system. For our present studies performed with the big brown bat (Eptesicus fuscus), we hypothesized that egocentric selection adjusts the frequency map of the inferior colliculus (IC) according to auditory experience based on associative learning. To test this hypothesis, we delivered acoustic stimuli paired with electric leg stimulation to the bat, because such paired stimuli allowed the animal to learn that the acoustic stimulus was behaviorally important and to make behavioral and neural adjustments based on the acquired importance of the acoustic stimulus. We found that acoustic stimulation alone evokes a change in the frequency map of the IC; that this change in the IC becomes greater when the acoustic stimulation is made behaviorally relevant by pairing it with electrical stimulation; that the collicular change is mediated by the corticofugal system; and that the IC itself can sustain the change evoked by the corticofugal system for some time. Our data support the hypothesis.The response properties of neurons in the subcortical auditory nuclei, as well as in the auditory cortex (AC) can be changed by associating an acoustic stimulus (conditioning stimulus: CS) with an electric foot stimulus (unconditioned stimulus). After conditioning, the response of neurons in the AC (1-3) and the medial geniculate body (MGB) of the adult guinea pig (4, 5) increases to the frequency of a CS tone, but decreases to other frequencies, including the original best frequencies (BFs) of the neurons. These changes result in a shift in BF toward the frequency of the CS tone. The BF shift lasts at least 8 weeks in the AC (3), at least 1 hr in the dorsal division of the MGB (4), and less than 1 hr in the ventral division of the MGB (5). In the rat, the response of neurons in the inferior colliculus (IC) increases to frequencies used for a discrimination task (6), and 2-deoxyglucose uptake in the IC increases in the iso-BF band representing the frequency of the CS tone (7). All of these studies indicate that information processing in the central auditory system can be modified by auditory experience.However, the neural mechanisms underlying these changes have mostly remained unexplored.Recent studies indicate that cortical neurons of the mustached bat (Pteronotus parnellii) mediate, via corticofugal projection, a highly focused positive feedback to subcortical neurons ''matched'' in tuning to a particular acoustic parameter and a widespread lateral inhibition to ''unmatched'' subcorti...

show abstract

Section: Discussionmentioning

confidence: 81%

Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system

Gao

Suga²

1998

Proc. Natl. Acad. Sci. U.S.A.

204

137

View full text Add to dashboard Cite

show abstract

“…Former studies in the somatosensory system have shown that cortical inactivation mainly depresses innocuous-evoked thalamic responses (Yuan et al, 1986;Diamond et al, 1992). More recent studies demonstrated that S1 can selectively modulate thalamic spatial responses through specific excitatory or inhibitory mechanisms that either sharpen or enlarge thalamic receptive fields (Ergenzinger et al, 1998;Ghazanfar et al, 2001;Temereanca and Simons, 2004).…”

Section: Discussionmentioning

confidence: 99%

“…The function of this massive feedback network in pain has not been fully studied. However, the influence of cortical modulation from S1 on the organization of whisker-barrel receptive fields in the ventroposteromedial thalamic nucleus (Krupa et al, 1999;Ghazanfar et al, 2001;Temereanca and Simons, 2004) and on the organization of limb tactile receptive fields in the ventroposterolateral nucleus (VPL) (Yuan et al, 1986;Ghosh et al, 1994;Ergenzinger et al, 1998) has been clearly established. As in the visual and auditory systems, corticofugal influences from S1 serves to amplify the effects of sensory stimulation to the classical center-surround receptive fields and helps to sharpen and adjust the profile of thalamic receptive fields (the "egocentric selection") (Rauschecker, 1998;Suga and Ma, 2003).…”

Section: Introductionmentioning

confidence: 99%

Corticofugal Output from the Primary Somatosensory Cortex Selectively Modulates Innocuous and Noxious Inputs in the Rat Spinothalamic System

et al. 2006

View full text Add to dashboard Cite

Sensory maps for pain can be modified by deafferentation or injury, and such plasticity has been attributed mainly to changes in the convergence of projections in "bottom-up" mechanisms. We addressed the possible contribution of "top-down" mechanisms by investigating the functional significance of corticofugal influences from the primary somatosensory cortex (S1) to the ventroposterolateral thalamic nucleus (VPL). The strong convergence of spinal and lemniscal afferents to the VPL and the close correspondence between afferents and efferents within the VPL-S1 network suggest the existence of functionally related thalamocortical circuits that are implicated in the detection of innocuous and noxious inputs. Functional characterization of single nociceptive, wide dynamic range, and non-nociceptive VPL neurons and labeling the axons and terminal fields with the juxtacellular technique showed that all three types of cells project to a restricted area, within S1. The convergence of the terminal trees of axons from VPL neurons activated by innocuous, noxious, or both inputs suggests that their inputs are not segregated into anatomically distinct regions. Microinjections within S1 were performed for pharmacological manipulation of corticofugal modulation. Glutamatergic activation of corticofugal output enhanced noxious-evoked responses and affected in a biphasic way tactile-evoked responses of VPL cells. GABA A -mediated depression of corticofugal output concomitantly depressed noxious and enhanced innocuous-evoked responses of VPL neurons. Microinjections of a GABA A antagonist on corticofugal cells enhanced noxious-evoked responses of VPL cells. Our findings demonstrate that corticofugal influences from S1 contribute to selectively modulate somatosensory submodalities at the thalamic level.

show abstract

“…Cortex and thalamus are heavily interconnected with reciprocal specificity (Jones, 1985). Although the predominate view is that thalamo-cortical projections dominate receptive field structure in cortex, evidence is mounting that corticothalamic projections can have potent effects on thalamic representation (Ergenzinger et al, 1998). Physiological columnar architecture appears to be purely a cortical phenomena with a basis in the distribution of thalamic efferents (Rausell and Jones, 1995), and the magnitude of breakdown of columnar architecture noted in this and previous studies of focal hand dystonia (Byl et al, 1996) has not been found in other normal or behaviorally trained primates in our or other laboratories.…”

Section: Thalamic Findings; Implications For Sites Of Plasticitymentioning

confidence: 99%

Sensory representation abnormalities that parallel focal hand dystonia in a primate model

Blake

Byl

Cheung

et al. 2002

Somatosensory & Motor Research

View full text Add to dashboard Cite

In our hypothesis of focal dystonia, attended repetitive behaviors generate aberrant sensory representations. Those aberrant representations interfere with motor control. Abnormal motor control strengthens sensory abnormalities. The positive feedback loop reinforces the dystonic condition. Previous studies of primates with focal hand dystonia have demonstrated multi-digit or hairyglabrous responses at single sites in area 3b, receptive fields that average ten times larger than normal, and high receptive field overlap as a function of horizontal distance. In this study, we strengthen and elaborate these findings. One animal was implanted with an array of micro-electrodes that spanned the border between the face and digits. After the animal developed hand dystonia, responses in the initial hand representation increasingly responded to low threshold stimulation of the face in a columnar substitution. The hand-face border that is normally sharp became patchy and smeared over one millimeter of cortex within six weeks. Two more trained animals developed a focal hand dystonia variable in severity across the hand. Receptive field size, presence of multi-digit or hairy-glabrous receptive fields, and columnar overlap covaried with the animal's ability to use specific digits. A fourth animal performed the same behaviors without developing dystonia. Many of its physiological measures were similar to the dystonic animals, but receptive field overlap functions were minimally abnormal, and no sites shared response properties that are normally segregated such as hairy-glabrous combined fields, or multi-digit fields. Thalamic mapping demonstrated proportionate levels of abnormality in thalamic representations as was found in cortical representations.

show abstract

Cortically induced thalamic plasticity in the primate somatosensory system

Cited by 149 publications

References 22 publications

Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system

Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system

Corticofugal Output from the Primary Somatosensory Cortex Selectively Modulates Innocuous and Noxious Inputs in the Rat Spinothalamic System

Sensory representation abnormalities that parallel focal hand dystonia in a primate model

Contact Info

Product

Resources

About