Lemniscal recurrent and transcortical influences on cuneate neurons

[Abstract] Intracellular recordings were obtained from cuneate neurons of chloralose-anesthetized, paralysed cats to study the synaptic responses induced by electrical stimulation of the contralateral medial lemniscus. From a total of 178 cells sampled, 109 were antidromically fired from the medial lemniscus, 82 of which showed spontaneous bursting activity. In contrast, the great majority (58/69) of the non-lemniscal neurons presented spontaneous single spike activity. Medial lemniscus stimulation induced recurrent excitation and inhibition on cuneolemniscal and non-lemniscal cells. Some non-lemniscal neurons were activated by somatosensory cortex and inhibited by motor cortex stimulation. Some other non-lemniscal cells that did not respond to medial lemniscus stimulation in control conditions were transcortically affected by stimulating the medial lemniscus after inducing paroxysmal activity in the sensorimotor cortex. These findings indicate that different sites in the sensorimotor cortex can differentially influence the sensory transmission through the cuneate, and that the distinct available corticocuneate routes are selected within the cerebral cortex. From a total of 92 cells tested, the initial effect induced by low-frequency stimulation of the sensorimotor cortex was inhibition on most of the cuneolemniscal neurons (32/52) and excitation on the majority of the non-lemniscal cells (25/40). The fact that a substantial proportion of cuneolemniscal and non-lemniscal cells was excited and inhibited, respectively, suggests that the cerebral cortex may potentiate certain inputs by exciting and disinhibiting selected groups of cuneolemniscal cells. Finally, evidence is presented demonstrating that the tendency of the cuneolemniscal neurons to fire in high-frequency spike bursts is due to different mechanisms, including excitatory synaptic potentials, recurrent activation through lemniscal axonal collaterals, and via the lemnisco-thalamo-cortico-cuneate loop. A corticocuneate network circuit to explain the results is proposed.Dirección General de Investigación Científica y Técnica; PB96-095

Cortico-subcortical synchronization in the chloralose-anesthetized cat

[Abstract] The spontaneous and paroxysmal cerebral cortical synchronized activity was used as reference to study the cortical impact exerted on subcortical neurons. The sensorimotor cortical synchronized activity spread down to subcortical structures receiving direct cortical input, including neuronal populations that originate descending rubrospinal, tectospinal and reticulospinal motor axons, and to a somatosensory relay station, the cuneate nucleus. Lesion of the pyramidal tract abolished the cortically induced synchronization of the activity of contralateral cuneate nucleus neurons.Ministerio de Educación y Ciencia; PB96-095

The lemniscal–cuneate recurrent excitation is suppressed by strychnine and enhanced by GABAA antagonists in the anaesthetized cat

[Abstract] In the somatosensory system, cuneolemniscal (CL) cells fire high frequency doublets of spikes facilitating the transmission of sensory information to diencephalic target cells. We studied how lemniscal feedback affects ascending transmission of cutaneous neurons of the middle cuneate nucleus. Electrical stimulation of the contralateral medial lemniscus and of the skin at sites evoking responses with minimal threshold induced recurrent activation of CL cells at a latency of 1–3.5 ms. The lemniscal feedback activation was suppressed by increasing the stimulating intensity at the same sites, suggesting recurrent-mediated lateral inhibition. The glycine antagonist strychnine blocked the recurrent excitatory responses while GABAA antagonists uncovered those obscured by stronger stimulation. CL cells sharing a common receptive field (RF) potentiate one another by recurrent activation and disinhibition, the disinhibition being produced by serial interactions between glycinergic and GABAergic interneurons. Conversely, CL cells with different RFs inhibit each other through recurrent GABA-mediated inhibition. The lemniscal feedback would thus enhance the surround antagonism of a centre response by increasing the spatial resolution and the transmission of weak signals.Consejo Interinstitucional de Ciencia y Tecnología; PM99-002

Sensorimotor cortical influences on cuneate nucleus rhythmic activity in the anesthetized cat

[Abstract] This work aimed to study whether the sensorimotor cerebral cortex spreads down its rhythmic patterns of activity to the dorsal column nuclei. Extracellular and intracellular recordings were obtained from the cuneate nucleus of chloralose-anesthetized cats. From a total of 140 neurons tested (106 cuneolemniscal), 72 showed spontaneous rhythmic activity within the slow (<1 Hz), δ (1–4 Hz), spindle (5–15 Hz) and higher frequencies, with seven cells having the δ rhythm coupled to slow oscillations. The spindle activity recorded in the cuneate was tightly coupled to the thalamo-cortico-thalamic spindle rhythmicity. Bilateral or contralateral removal of the frontoparietal cortex abolished the cuneate slow and spindle oscillations. Oscillatory paroxysmal activity generated by fast electrical stimulation (50–100 Hz/1–2 s) of the sensorimotor cortex induced burst firing synchronized with the paroxysmal cortical “spike” on all the non-lemniscal neurons, and inhibitory responses also coincident with the cortical paroxysmal “spike” in the majority (71%) of the cuneolemniscal cells. The remaining lemniscal-projecting neurons showed bursting activity (11%) or sequences of excitation–inhibition (18%) also time-locked to the cortical paroxysmal “spike”. Additionally, the cerebral cortex induced coherent oscillatory activity between thalamic ventroposterolateral and cuneate neurons. Electrolytic lesion of the pyramidal tract abolished the cortically induced effects on the contralateral cuneate nucleus, as well as on the ipsilateral medial lemniscus. The results demonstrate that the sensorimotor cortex imposes its rhythmic patterns on the cuneate nucleus through the pyramidal tract, and that the corticocuneate network can generate normal and abnormal patterns of synchronized activity, such as δ waves, spindles and spike-and-wave complexes. The cuneate neurons, however, are able to generate oscillatory activity above 1 Hz in the absence of cortical input, which implies that the cerebral cortex probably imposes its rhythmicity on the cuneate by matching the intrinsic preferred oscillatory frequency of cuneate neurons.Dirección General de Investigación Científica y Técnica; PB96-095

Coupled slow and delta oscillations between cuneothalamic and thalamocortical neurons in the chloralose anesthetized cat

Simultaneous recordings were obtained from cuneothalamic (extracellular) and thalamocortical (intracellular) cells in chloralose anesthetized cats. It was found that cuneothalamic neurons present slow rhythmicity (0.1–1 Hz) tightly coupled to slow oscillations of thalamocortical neurons. This coupling was not due to a direct synaptic linkage but rather produced by other (s) structure (s) probably the cortex. Furthermore, the cuneothalamic neurons also showed delta rhythms (1–4 Hz) coherently oscillating with the delta rhythms of thalamocortical cells which suggests that these rhythms are more widespread than previously thought, and may be a general phenomenon characterizing quiet sleep in multiple structures

Tonic and bursting activity in the cuneate nucleus of the chloralose-anesthetized cat

[Abstract] Whole-cell recordings were obtained from cuneate neurons in anesthetized, paralysed cats. Stimulation of the contralateral medial lemniscus permitted us to separate projection cells from presumed interneurons. Pericruciate motor cortex electrical stimulation inhibited postsynaptically all the projection cells (n=57) and excited all the presumed interneurons (n=29). The cuneothalamic cells showed an oscillatory and a tonic mode of activity. Membrane depolarization and primary afferent stimulation converted the oscillatory to the tonic mode. Hyperpolarizing current steps applied to projection neurons induced a depolarizing sag and bursts of conventional spikes in current-clamp records. This indicates the probable existence of low-threshold and hyperpolarization-activated inward currents. Also, the hyperpolarization induced on projection cells by motor cortex stimulation deinactivated a low-threshold conductance that led to bursting activity. The presumed cuneate interneurons had larger and more proximally located peripheral receptive fields than the cuneothalamic cells. Finally, experiments specifically designed to test whether motor cortex-induced presynaptic inhibition could be postsynaptically detected gave negative results. These results demonstrate, for the first time, that the cuneothalamic cells possess both bursting and tonic firing modes, and that membrane depolarization, whether produced by injection of positive current or by primary afferent stimulation, converts the oscillatory into the tonic mode.Dirección General de Investigación Científica y Técnica; PB93-034

La corteza cerebral modula la transmisión cutánea a través de los núcleos de los cordones posteriores

The mechanisms used by the cerebral cortex to modulate the cutaneous information at prethalamic level have been scarcely studied. This article reviews experimental evidence leading to a better understanding of this issue at the level of the cuneate nucleus (Burdach nucleus). Development. The primary afferents and the corticocuneate fibers make synaptic contact with cuneothalamic neurons and with inhibitory interneurons in the middle cuneate nucleus. By stimulating the skin at different places while recording the cuneothalamic intracellular activity in anaesthetized animals with the cortex intact, with the cortex pharmacologically inactivated, or in absence of a cerebral cortex it was possible to ascertain the functional role of the corticocuneate fibers. The primary afferents activated by stimulating a particular zone of the skin induce monosynaptic excitation on a group of cuneothalamic cells at the same time at which inhibit, through intranuclear interneurons, neighboring cuneothalamic cells with unmatched receptive fields. Similarly, the corticocuneate cells receiving information from the stimulated skin further increase the excitation of the cuneothalamic neurons with matched receptive fields while inhibiting others with unmatched fields. The cortex exaggerates an excited center surrounded by an inhibited periphery thus increasing the tactile discrimination both spatially and temporally which is essential for exploratory and manipulative purpose

The role of glyclinergic interneurons in the dorsal column nuclei

[Abstract] The aim of this paper is to provide new insights about the circuitry and the role of the dorsal column nuclei (DCN) in processing somatosensory information. The presence of glycinergic cells, a second type of DCN interneurons in addition to well-known GABAergic interneurons, opens the door to more complex interactions between cuneate cells as well as to a new hypothesis about the computational implications of such interactions. The research posed here fits in a broader context in the field of the sensory systems and deals with the general issue on the role of subcortical structures (i.e the thalamus) in processing sensory information

Sleep and wakefulness in the cuneate nucleus: a computational study

We present a computational study about the influence of the sensorimotor cortex on the processing of the cuneate nucleus during sleep as well as wakefulness. Realistic computational models were developed supported by experimental data obtained from intact-brain preparations in cat. Furthermore, a physiologically plausible circuit is proposed and predictions under both different cortical stimulation and synaptic configurations are suggested. The computer simulations show that the CN circuitry (1) under sleep conditions can block the transmission of afferent sensory information, and (2) under awaking conditions can perform operations such as filtering and facilitation

Intracuneate mechanisms underlying primary afferent cutaneous processing in anaesthetized cats

[Abstract] The cutaneous primary afferents from the upper trunk and forelimbs reach the medial cuneate nucleus in their way towards the cerebral cortex. The aim of this work was twofold: (i) to study the mechanisms used by the primary afferents to relay cutaneous information to cuneate cuneolemniscal (CL) and noncuneolemniscal (nCL) cells, and (ii) to determine the intracuneate mechanisms leading to the elaboration of the output signal by CL cells. Extracellular recordings combined with microiontophoresis demonstrated that the primary afferent cutaneous information is communicated to CL and nCL cells through AMPA, NMDA and kainate receptors. These receptors were sequentially activated: AMPA receptors participated mainly during the initial phase of the response, whereas kainate- and NMDA-mediated activity predominated during a later phase. The involvement of NMDA receptors was confirmed by in vivo intracellular recordings. The cutaneous-evoked activation of CL cells was decreased by GABA and increased by glycine acting at a strychnine-sensitive site, indicating that glycine indirectly affects CL cells. Two subgroups of nCL cells were distinguished based on their sensitivity to iontophoretic ejection of glycine and strychnine. Overall, the results support a model whereby the primary afferent cutaneous input induces a centre-surround antagonism in the cuneate nucleus by activating (via AMPA, NMDA and kainate receptors) and disinhibiting (via serial glycinergic–GABAergic interactions) a population of CL cells with overlapped receptive fields that at the same time inhibit (via GABAergic cells) other neighbouring CL cells with different receptive fields.Ministerio de Ciencia y Tecnología; BFI 2003-0194