Zona incerta

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Zona incerta
Details
Identifiers
Latin zona incerta
MeSH D065820
TA98 A14.1.08.707
TA2 5707
FMA 62038
Anatomical terms of neuroanatomy

The zona incerta (ZI) is a horizontally elongated region of gray matter in the subthalamus below the thalamus. Its connections project extensively over the brain from the cerebral cortex down into the spinal cord.

Contents

Its function is unknown, though several potential functions related to "limbic–motor integration" have been proposed, such as controlling visceral activity and pain; gating sensory input and synchronizing cortical and subcortical brain rhythms. Its dysfunction may play a role in central pain syndrome. It has also been identified as a promising deep brain stimulation therapy target for treating Parkinson's disease.

Its existence was first described by Auguste Forel in 1877 as a "region of which nothing certain can be said". [1] [2] A hundred and thirty years later in 2007, Nadia Urbain and Martin Deschênes of Université Laval noted that the "zona incerta is among the least studied regions of the brain; its name does not even appear in the index of many textbooks." [3]

Structure

The zona incerta is situated between the lateral medullary lamina, and the cerebral peduncle. It extends between rostral pole of the thalamus rostrally, and the rostral pole of the medial geniculate nucleus caudally. [4] This nucleus is located medially to the internal capsule, ventral to the thalamus, and is contiguous with the thalamic reticular nucleus. [5] The nucleus separates the lenticular fasciculus from the thalamic fasciculus (also known as the "field H1 of Forel") . Its cells are very heterogeneous differing widely in their shape and size. Its chemoarchitecture is also diverse containing up to 20 different types of neurochemically defined cells. It has been noted that "There are few diencephalic regions that have as much cellular and neurochemical diversity". [2]

In the rat four areas are usually identified. [6] [7] [8]

These areas lack clear cell-free borders and merge into each other. [2]

Zona incerta neurons have dendrites with a wide span 0.8 mm and their axons give off collaterals that arborized locally within the zona incerta providing a means for lateral inhibition. The ventral area of the zona incerta has been described as having "a network of GABAergic cells with widespread interconnections, so that cells in one subsector may influence the activity of cells in a different subsector". [3]

The zona incerta together with the hypothalamus is one of the two areas of the brain that produces the neuropeptide melanin concentrating hormone. [10] Dopaminergic ones are also more prevalent. [8] There are in addition populations of cells producing somatostatin, angiotensin II and melanocyte stimulating hormone. [8]

Connections

The zona incerta has connections to the cerebral cortex, diencephalon, basal ganglia, brainstem and spinal cord.

Cerebral cortex

Projections to the zona incerta arise across the cortical mantel from the frontal to the occipital lobes. The heaviest projections are from cingulate cortex, frontal and parietal areas, but also projections from the medial prefrontal cortex have been reported. The head area of the body seems from these areas to have the largest representation in the zona incerta. These projections preferentially go to cortical layer I neurons. [11] There are projections from the zona incerta back to the cerebral cortex. [12] [13]

Diencephalon

Projections with the diencephalon are reciprocal and mainly to the thalamus such as the intralaminar nucleus (parafascicular nucleus and central lateral nucleus) and higher-order nuclei such as the lateral posterior nucleus. The zona incerta avoids the thalamus nuclei of the primary sensory areas such as the ventral posterior nucleus of the somatosensory system and the lateral geniculate of the visual system. [14] Rostral zona incerta also sends inhibitory projections to paraventricular thalamus with GABAergic neurotransmission. [15]

Hypothalamus

Projections to the hypothalamus through incertohypothalamic pathway go mainly to the paraventricular nucleus areas in the anterior hypothalamus, lateral hypothalamus, lateral preoptic area, horizontal diagonal band of Broca, and the parvocellular region of the paraventricular nucleus. [16]

Basal ganglia

Zona incerta is connected in the basal ganglia to the substantia nigra (both pars compacta and pars reticulata) and pedunculopontine tegmental nucleus (but only its pars dissipata area). It also has less important connections to the entopeduncular nucleus and globus pallidus. These projections are glutamatergic and excitatory rather than GABAergic and inhibitory. [17] The zona incerta also receives input from these areas.

Cerebellum

The cerebellum sends a significant number of fibers to the zona incerta. [18] These projections originate from various cerebellar nuclei and are glutamatergic. Given the cerebellar contributions to motor learning, timing and coordination, the interactions between the cerebellum with the zona incerta are likely to have profound influence on motor functions.

Brainstem

Zona incerta receives input from many parts of the brainstem nuclei including the periaqueductal gray, raphe nuclei, thalamic reticular nucleus, and the deep layers of the superior colliculus. It is regulated by inputs from brainstem cholinergic nuclei such as the Laterodorsal tegmental nucleus and pedunculopontine nucleus upon its neuron’s muscarinic receptors. The rostral zona incerta also innervates the dorsolateral and ventrolateral compartments of the periaqueductal gray. [19] [20]

Spinal cord

Zona incerta afferents terminate within the spinal cord gray matter, particularly the anterior horn, while spinal projections back to the zona incerta arise from cells located across the posterior horn and intermediate gray.

Other

Zona incerta also has connections to the amygdala, basal forebrain, the osmoreceptors in the subfornical organ, olfactory bulb, posterior pituitary and habenula.

Some of these projections appear in register; the representation of the same body part in cortex and spinal cord connect to the same areas in the zona incerta. [21] This is possibly so with the superior colliculus. [22]

Function

Visceral survival activities

Zona incerta controls such activities as water and food intake, sexuality and cardiovascular activity. This control is related to its effects upon the nearby posterior hypothalamus with which it shares similar connections and neurochemically defined cell types. [2] Activation of GABA neurons in rostral zona incerta evokes binge eating behavior with a preference to sweet and high-fat food. The inhibitory projection from zona incerta to paraventricular thalamus contributes to binge-like eating produced by zona incerta GABA neuron activation. [15]

Zona incerta has also been found to modulate both innate and learned defensive behaviors through its projections to the excitatory neurons of the dorsolateral and ventrolateral compartments of the periaqueductal gray. Activation of the GABAergic neurons in the rostral zona incerta reduces sound-induced innate flight response and conditioned freezing response. [23]

The zona incerta receives pain input through the spinothalamic tract and this has been shown to control the activity of the pain transmission pathway in the posterior thalamus. [14]

Electrical or chemical stimulation of the zona incerta creates limbic-related movements, such as those associated with defense orientation and copulation. [24]

Sensory-motor activities

At rest sensory input to the higher sensory areas of the cerebral cortex is gated through the thalamus. It has moreover been proposed that the zona incerta provides a top-down disinhibitory mechanism of this gating when there is sensory-motor activity such as the tactile use of whiskers. [3] [25]

This has also been linked to sensory gating changes between sleep and waking. In this occurs a zona incerta mediated inhibition of thalamic nuclei such the somatosensory posterior medial thalamus. This is most strong when cholinergic input to the zona incerta is reduced as during slow-wave sleep and during anesthesia. The consequence of this has been explained upon information processing:

As a result, posterior medial thalamus neurons fail to respond to ascending sensory inputs, and function primarily in "higher-order" mode, concerned with relaying trans-cortical information. By contrast, increased cholinergic activity during wakefulness and enhanced vigilance suppresses zona incerta -mediated inhibition, thereby ungating posterior thalamus responses to ascending inputs. [19]

The zona incerta projects to the superior colliculus and these link to the initiation of orientating eye and head movements. In monkeys for example neuronal activity in the zona incerta "pauses" before the start of a saccade and resumes at the end of a saccade. [26]

Synchronizing cortical and subcortical brain rhythms and integration

The GABAergic input received from the cerebral cortex has been suggested to synchronize thalamocortical and brainstem rhythms by providing a link between basal ganglia output and the cerebello-thalamo cortical loop. [9] [27] This allows it to synchronize oscillations generate by the basal ganglia during the preparation and execution of intended movements. One function of the loop is to carry movement instructions to the motor cortex through zona incerta output to the ventral lateral nucleus neurons in the cerebello-thalamocortical loop and to brainstem motor neurons in the medial reticular formation and midbrain extrapyramidal area. This acts to synchronize the basal ganglia areas involved in planning and execution of the movement with those in the brainstem controlling axial and proximal limb muscles with those areas in the motor cortex that control distal limb movements. [9]

Synthesis

John Mitrofanis at the University of Sydney has proposed a general theory that might underlie some of the above.

The zona incerta is in a position to form a primal synaptic interface of the diencephalon, linking diverse sensory channels to appropriate visceral, arousal, attention and posture-locomotion responses. The different sensory inputs, whether exteroreceptive (somatic) or interoreceptive (visceral), influence these activities by driving zona incerta cells with different projection patterns and functions; each of these cells may be located in different sectors of the zone… In essence, it is suggested that the zona incerta has the pathways to integrate both exteroreceptive (e.g. somatosensory) and interoreceptive (e.g. thirst) sensory challenges, so that visceral activity, arousal, attention and/or posture locomotion are altered and/or generated. The zona incerta could form a neural niche in the thalamus from where these responses are "recruited" immediately, as to give an instant response. [2]

Clinical significance

Parkinson's disease

Parkinson's disease might disrupt the zona incerta as it is hyperactive in parkinsonian experimental animals. [28] In humans with Parkinson's disease, surgical lesion of the zona incerta alleviates their parkinsonian motor symptoms.

Deep brain stimulation of the subthalamic nucleus in those with Parkinson's disease has identified the zona incerta as a promising target area for effective therapy. [29] Unlike deep bilateral stimulation of the ventral lateral nucleus such stimulation of the zona incerta improves all aspects of tremor including both the distal and proximal parts of limbs and the body more generally. [9] This also occurs without dysarthria and disequilibrium as this stimulation does not interrupt proprioceptive sensation and the processing of the fine motor skill movements of vocal cords.

Researchers observed that "The ventral lateral nucleus has long been established as an effective surgical target for controlling distal limb tremor, including Parkinson Disease tremor. However, because it receives predominantly cerebellar afferents and no direct basal ganglia afferents, the reason why it is effective in controlling Parkinson Disease tremor has remained a paradox. The conduction of abnormal oscillations generated in the basal ganglia in Parkinson Disease to the ventral lateral nucleus via zona incerta would therefore explain this paradox and also explain why we observed such a potent anti-tremor effect from stimulating zona incerta in our patients with Parkinson Disease" [9]

The study further noted that deep brain stimulation upon the zona incerta "is effective in suppressing all components of tremor affecting both the distal and proximal part of the body. These results, if replicated in larger randomised controlled studies, have important implications for our current surgical management of patients with tremor and point to a more promising target area than the ventral lateral nucleus of the thalamus." [9]

Central pain syndrome

Central pain syndrome is pain initiated or caused by injury or dysfunction in the central nervous system. Recent research suggests that the development and maintenance of such pain could link to abnormal inhibitory regulation by the zona incerta of the posterior thalamus. [14] It has been suggested that there exists

a significant suppression of both spontaneous and evoked activity in inhibitory neurons in zona incerta and abnormally high spontaneous and evoked activity of neurons in posterior thalamus in animals with central pain syndrome. The positive association between behavioral and neurophysiological thresholds in rats with central pain syndrome is consistent with a causal role for suppressed incerto-thalamic inputs in central pain syndrome. [14]

Related Research Articles

<span class="mw-page-title-main">Substantia nigra</span> Structure in the basal ganglia of the brain

The substantia nigra (SN) is a basal ganglia structure located in the midbrain that plays an important role in reward and movement. Substantia nigra is Latin for "black substance", reflecting the fact that parts of the substantia nigra appear darker than neighboring areas due to high levels of neuromelanin in dopaminergic neurons. Parkinson's disease is characterized by the loss of dopaminergic neurons in the substantia nigra pars compacta.

<span class="mw-page-title-main">Thalamus</span> Structure within the brain

The thalamus is a large mass of gray matter located in the dorsal part of the diencephalon. Nerve fibers project out of the thalamus to the cerebral cortex in all directions, known as the thalamocortical radiations, allowing hub-like exchanges of information. It has several functions, such as the relaying of sensory signals, including motor signals to the cerebral cortex and the regulation of consciousness, sleep, and alertness.

<span class="mw-page-title-main">Basal ganglia</span> Group of subcortical nuclei involved in the motor and reward systems

The basal ganglia (BG) or basal nuclei are a group of subcortical nuclei found in the brains of vertebrates. In humans and other primates, differences exist, primarily in the division of the globus pallidus into external and internal regions, and in the division of the striatum. Positioned at the base of the forebrain and the top of the midbrain, they have strong connections with the cerebral cortex, thalamus, brainstem and other brain areas. The basal ganglia are associated with a variety of functions, including regulating voluntary motor movements, procedural learning, habit formation, conditional learning, eye movements, cognition, and emotion.

<span class="mw-page-title-main">Brainstem</span> Posterior part of the brain, adjoining and structurally continuous

The brainstem is the stalk-like part of the brain that interconnects the cerebrum and diencephalon with the spinal cord. In the human brain, the brainstem is composed of the midbrain, the pons, and the medulla oblongata. The midbrain is continuous with the thalamus of the diencephalon through the tentorial notch.

<span class="mw-page-title-main">Spinothalamic tract</span> Sensory pathway from the skin to the thalamus

The spinothalamic tract is a part of the anterolateral system or the ventrolateral system, a sensory pathway to the thalamus. From the ventral posterolateral nucleus in the thalamus, sensory information is relayed upward to the somatosensory cortex of the postcentral gyrus.

<span class="mw-page-title-main">Dorsal column–medial lemniscus pathway</span> Sensory spinal pathway

The dorsal column–medial lemniscus pathway (DCML) is a sensory pathway of the central nervous system that conveys sensations of fine touch, vibration, two-point discrimination, and proprioception from the skin and joints. It transmits information from the body to the primary somatosensory cortex in the postcentral gyrus of the parietal lobe of the brain. The pathway receives information from sensory receptors throughout the body, and carries this in nerve tracts in the white matter of the dorsal column of the spinal cord to the medulla, where it is continued in the medial lemniscus, on to the thalamus and relayed from there through the internal capsule and transmitted to the somatosensory cortex. The name dorsal-column medial lemniscus comes from the two structures that carry the sensory information: the dorsal columns of the spinal cord, and the medial lemniscus in the brainstem.

<span class="mw-page-title-main">Dopaminergic pathways</span> Projection neurons in the brain that synthesize and release dopamine

Dopaminergic pathways in the human brain are involved in both physiological and behavioral processes including movement, cognition, executive functions, reward, motivation, and neuroendocrine control. Each pathway is a set of projection neurons, consisting of individual dopaminergic neurons.

<span class="mw-page-title-main">Nigrostriatal pathway</span> Bilateral pathway in the brain

The nigrostriatal pathway is a bilateral dopaminergic pathway in the brain that connects the substantia nigra pars compacta (SNc) in the midbrain with the dorsal striatum in the forebrain. It is one of the four major dopamine pathways in the brain, and is critical in the production of movement as part of a system called the basal ganglia motor loop. Dopaminergic neurons of this pathway release dopamine from axon terminals that synapse onto GABAergic medium spiny neurons (MSNs), also known as spiny projection neurons (SPNs), located in the striatum.

<span class="mw-page-title-main">Ventral tegmental area</span> Group of neurons on the floor of the midbrain

The ventral tegmental area (VTA), also known as the ventral tegmental area of Tsai, or simply ventral tegmentum, is a group of neurons located close to the midline on the floor of the midbrain. The VTA is the origin of the dopaminergic cell bodies of the mesocorticolimbic dopamine system and other dopamine pathways; it is widely implicated in the drug and natural reward circuitry of the brain. The VTA plays an important role in a number of processes, including reward cognition and orgasm, among others, as well as several psychiatric disorders. Neurons in the VTA project to numerous areas of the brain, ranging from the prefrontal cortex to the caudal brainstem and several regions in between.

<span class="mw-page-title-main">Pretectal area</span> Structure in the midbrain which mediates responses to ambient light

In neuroanatomy, the pretectal area, or pretectum, is a midbrain structure composed of seven nuclei and comprises part of the subcortical visual system. Through reciprocal bilateral projections from the retina, it is involved primarily in mediating behavioral responses to acute changes in ambient light such as the pupillary light reflex, the optokinetic reflex, and temporary changes to the circadian rhythm. In addition to the pretectum's role in the visual system, the anterior pretectal nucleus has been found to mediate somatosensory and nociceptive information.

<span class="mw-page-title-main">Reticular formation</span> Spinal trigeminal nucleus

The reticular formation is a set of interconnected nuclei that are located throughout the brainstem. It is not anatomically well defined, because it includes neurons located in different parts of the brain. The neurons of the reticular formation make up a complex set of networks in the core of the brainstem that extend from the upper part of the midbrain to the lower part of the medulla oblongata. The reticular formation includes ascending pathways to the cortex in the ascending reticular activating system (ARAS) and descending pathways to the spinal cord via the reticulospinal tracts.

<span class="mw-page-title-main">Thalamocortical radiations</span> Neural pathways between the thalamus and cerebral cortex

In neuroanatomy, thalamocortical radiations, also known as thalamocortical fibres, are the efferent fibres that project from the thalamus to distinct areas of the cerebral cortex. They form fibre bundles that emerge from the lateral surface of the thalamus.

<span class="mw-page-title-main">Primate basal ganglia</span>

The basal ganglia form a major brain system in all species of vertebrates, but in primates there are special features that justify a separate consideration. As in other vertebrates, the primate basal ganglia can be divided into striatal, pallidal, nigral, and subthalamic components. In primates, however, there are two pallidal subdivisions called the external globus pallidus (GPe) and internal globus pallidus (GPi). Also in primates, the dorsal striatum is divided by a large tract called the internal capsule into two masses named the caudate nucleus and the putamen—in most other species no such division exists, and only the striatum as a whole is recognized. Beyond this, there is a complex circuitry of connections between the striatum and cortex that is specific to primates. This complexity reflects the difference in functioning of different cortical areas in the primate brain.

<span class="mw-page-title-main">Medium spiny neuron</span> Type of GABAergic neuron in the striatum

Medium spiny neurons (MSNs), also known as spiny projection neurons (SPNs), are a special type of GABAergic inhibitory cell representing 95% of neurons within the human striatum, a basal ganglia structure. Medium spiny neurons have two primary phenotypes : D1-type MSNs of the direct pathway and D2-type MSNs of the indirect pathway. Most striatal MSNs contain only D1-type or D2-type dopamine receptors, but a subpopulation of MSNs exhibit both phenotypes.

<span class="mw-page-title-main">Gustatory nucleus</span> Rostral part of the solitary nucleus located in the medulla

The gustatory nucleus is the rostral part of the solitary nucleus located in the medulla. The gustatory nucleus is associated with the sense of taste and has two sections, the rostral and lateral regions. A close association between the gustatory nucleus and visceral information exists for this function in the gustatory system, assisting in homeostasis - via the identification of food that might be possibly poisonous or harmful for the body. There are many gustatory nuclei in the brain stem. Each of these nuclei corresponds to three cranial nerves, the facial nerve (VII), the glossopharyngeal nerve (IX), and the vagus nerve (X) and GABA is the primary inhibitory neurotransmitter involved in its functionality. All visceral afferents in the vagus and glossopharyngeal nerves first arrive in the nucleus of the solitary tract and information from the gustatory system can then be relayed to the thalamus and cortex.

<span class="mw-page-title-main">External globus pallidus</span> Part of the globus pallidus

The external globus pallidus combines with the internal globus pallidus (GPi) to form the globus pallidus, an anatomical subset of the basal ganglia. Globus pallidus means "pale globe" in Latin, indicating its appearance. The external globus pallidus is the segment of the globus pallidus that is relatively further (lateral) from the midline of the brain.

<span class="mw-page-title-main">Internal globus pallidus</span>

The internal globus pallidus and the external globus pallidus (GPe) make up the globus pallidus. The GPi is one of the output nuclei of the basal ganglia. The GABAergic neurons of the GPi send their axons to the ventral anterior nucleus (VA) and the ventral lateral nucleus (VL) in the dorsal thalamus, to the centromedian complex, and to the pedunculopontine complex.

<span class="mw-page-title-main">Basal ganglia disease</span> Group of physical problems resulting from basal ganglia dysfunction

Basal ganglia disease is a group of physical problems that occur when the group of nuclei in the brain known as the basal ganglia fail to properly suppress unwanted movements or to properly prime upper motor neuron circuits to initiate motor function. Research indicates that increased output of the basal ganglia inhibits thalamocortical projection neurons. Proper activation or deactivation of these neurons is an integral component for proper movement. If something causes too much basal ganglia output, then the ventral anterior (VA) and ventral lateral (VL) thalamocortical projection neurons become too inhibited, and one cannot initiate voluntary movement. These disorders are known as hypokinetic disorders. However, a disorder leading to abnormally low output of the basal ganglia leads to reduced inhibition, and thus excitation, of the thalamocortical projection neurons which synapse onto the cortex. This situation leads to an inability to suppress unwanted movements. These disorders are known as hyperkinetic disorders.

<span class="mw-page-title-main">Blocq's disease</span> Loss of memory of specialized movements causing the inability to maintain an upright posture

Blocq's disease was first considered by Paul Blocq (1860–1896), who described this phenomenon as the loss of memory of specialized movements causing the inability to maintain an upright posture, despite normal function of the legs in the bed. The patient is able to stand up, but as soon as the feet are on the ground, the patient cannot hold himself upright nor walk; however when lying down, the subject conserved the integrity of muscular force and the precision of movements of the lower limbs. The motivation of this study came when a fellow student Georges Marinesco (1864) and Paul published a case of parkinsonian tremor (1893) due to a tumor located in the substantia nigra.

The parafacial zone (PZ) is a brain structure located in the brainstem within the medulla oblongata believed to be heavily responsible for non-rapid eye movement (non-REM) sleep regulation, specifically for inducing slow-wave sleep.

References

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  23. ↑ Chou, Xiao-lin; Wang, Xiyue; Zhang, Zheng-gang; Shen, Li; Zingg, Brian; Huang, Junxiang; Zhong, Wen; Mesik, Lukas; Zhang, Li I.; Tao, Huizhong Whit (December 2018). "Inhibitory gain modulation of defense behaviors by zona incerta". Nature Communications. 9 (1): 1151. doi:10.1038/s41467-018-03581-6. ISSN   2041-1723. PMC   5861117 . PMID   29559622.
  24. ↑ Edwards, DA; Isaacs, S (1991). "Zona incerta lesions: effects on copulation, partner-preference and other socio-sexual behaviors". Behavioural Brain Research. 44 (2): 145–50. doi:10.1016/S0166-4328(05)80019-1. PMID   1751005. S2CID   4047364.
  25. ↑ Lavallée, P.; Urbain, N.; Dufresne, C.; Bokor, H.; Acsády, L.; Deschênes, M. (Aug 2005). "Feedforward inhibitory control of sensory information in higher-order thalamic nuclei". Journal of Neuroscience. 25 (33): 7489–7498. doi:10.1523/JNEUROSCI.2301-05.2005. ISSN   0270-6474. PMC   2670454 . PMID   16107636.
  26. ↑ Ma, T. P. (Nov 1996). "Saccade-related omnivectoral pause neurons in the primate zona incerta". NeuroReport. 7 (15–17): 2713–2716. doi:10.1097/00001756-199611040-00061. ISSN   0959-4965. PMID   8981453.
  27. ↑ Barthó, P.; Slézia, A.; Varga, V.; Bokor, H.; Pinault, D.; Buzsáki, G.; Acsády, L. (Feb 2007). "Cortical control of zona incerta". Journal of Neuroscience. 27 (7): 1670–1681. doi:10.1523/JNEUROSCI.3768-06.2007. ISSN   0270-6474. PMC   2670453 . PMID   17301175.
  28. ↑ Périer, C; Vila, M; Féger, J; Agid, Y; Hirsch, EC (2000). "Functional activity of zona incerta neurons is altered after nigrostriatal denervation in hemiparkinsonian rats". Experimental Neurology. 162 (1): 215–24. doi:10.1006/exnr.1999.7331. PMID   10716902. S2CID   8452646.
  29. ↑ Sun, A.; Yu, H.; Spooner, J.; Tatsas, D.; Davis, T.; Abel, W.; Kao, C.; Konrad, E. (August 2008). "Postmortem analysis following 71 months of deep brain stimulation of the subthalamic nucleus for Parkinson disease". Journal of Neurosurgery. 109 (2): 325–329. doi:10.3171/JNS/2008/109/8/0325. ISSN   0022-3085. PMID   18671648.
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