Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta

doi:10.1016/j.neuroscience.2004.08.017

Neuroscience

Volume 130, Issue 1, 2005, Pages 1-15

https://doi.org/10.1016/j.neuroscience.2004.08.017 Get rights and content

Abstract

The zona incerta (ZI), first described over a century ago by Auguste Forel as a “region of which nothing certain can be said,” forms a collection of cells that derives from the diencephalon. To this day, we are still not certain of the precise function of this “zone of uncertainty” although many have been proposed, from controlling visceral activity to shifting attention and from influencing arousal to maintaining posture and locomotion. In this review, I shall outline the recent advances in the understanding of the structure, connectivity and functions of the ZI. I will then focus on a possible and often neglected global role for the ZI, one that links its diverse functions together. In particular, I aim to highlight the idea that the ZI forms a primal center of the diencephalon for generating direct responses (visceral, arousal, attention and/or posture–locomotion) to a given sensory (somatic and/or visceral) stimulus. With this global role in mind, I will then address recent results indicating that abnormal ZI activity manifests in clinical symptoms of Parkinson disease.

Section snippets

Cytoarchitecture

The ZI forms a heterogeneous collection of cells. In many areas, cells of similar shape and size are clustered together, forming somewhat distinct regions or sectors. The precise number of these sectors varies between authors, however, from two to six in rats (see Gurdjian, 1927; Kuzemensky, 1977; Kawana and Watanabe, 1981; Watanabe and Kawana, 1982; Romanowski et al., 1985; Nicolelis et al., 1992, 1995; Kolmac and Mitrofanis, 1999a), from two to four in monkeys (Ma et al., 1992; Paxinos et

Summary

The ZI is made up by a heterogeneous collection of cells that can be divided into cytoarchitectonic sectors. These sectors are not clearly defined, however. In order to discern sector borders more clearly, other methods such as immunohistochemistry and/or tract-tracing should be used (see below).

Chemoarchitecture

The ZI has a rich tapestry of neurochemically distinct cells, most of which have been identified by immunohistochemistry. Some immunohistochemical markers define sector boundaries very well, while others do not. Two examples of neurochemicals that define sectors well are shown in Figs. 2 and 3A, B. Parvalbumin (Pv)⁺ cells are located principally in the ZIv (Figs. 2E, F, 3A), while nitric oxide synthase (NOs)⁺ cells concentrate in the ZId (Figs. 2G, H, 3B; Nicolelis et al., 1995; Kolmac and

Summary

There are some immunohistochemical markers that define sector borders very well (e.g. Pv, NOs) while there are others that do not (e.g. Glu, calbindin D28k). Although particular neurochemically defined cells tend to concentrate within a given sector, such cells are always found in other sectors in most cases (Fig. 3). There is no neurochemical marker reported to date that defines all the cells of a sector exclusively (Nicolelis et al., 1995; Kolmac and Mitrofanis, 1999a). At present, the border

Connections

One of the striking features of the ZI lies in its widespread connectivity with nearly all neural centers (Fig. 1). In general, the ZI connections with a given neural center are rarely limited to one sector; they usually involve two, often three. However, as with the chemoarchitecture, some sets of connections define sector boundaries better than others. For example, a tracer injection into the superior colliculus reveals retrogradely labeled ZI cells limited to the ZIv and defines the border

Summary

There is a heavy sensory—both exteroceptive (e.g. somatosensory) and interoceptive (e.g. ingestive)—input to the ZI from various neural centers, for example the spinal cord, many brainstem nuclei and subfornical region. There are also considerable inputs from motor centers, such as the cerebellum and particular brainstem nuclei (e.g. red nucleus). In terms of outputs, the ZI projects heavily to the thalamus, hypothalamus, brainstem and perhaps the cortex as well. Most ZI connections, associated

Functions

Over the years, there have been many studies—electrophysiological, pharmacological and ablation/lesion—that have explored the function of the ZI. From these reports, four major functions have emerged for the ZI, namely controlling visceral activity, influencing arousal, shifting attention and maintaining posture and locomotion. For this review, I will focus on these.

Visceral activity

Many functional studies have provided evidence that the ZI has a role in controlling visceral activity, in particular ingestion, sexual cycles and cardiovascular activities. Some of these studies are based on lesion (chemical or electrical) of the ZI. These results should be treated with some caution for two reasons. First, the spread of the toxin from the injection site may not have been limited to the ZI, spreading to adjacent areas (e.g. subthalamus, hypothalamus), and second, the ZI is

Arousal

The ZI has long been linked with an arousal-type function, mainly because of its heavy interconnections with the major arousal centers of the brainstem and thalamus (see previous section). Further, the ZI houses many Enk cells that are numerous in arousal associated nuclei (e.g. intralaminar; Hermanson et al., 1995). On these grounds, it has been suggested that the ZI forms an integral part of an arousal network circuit (Shammah-Lagnado et al., 1985; Berry et al., 1986; Kolmac et al., 1998;

Attention

Classically, the function of the ZI has been associated closely with that of the superior colliculus. In particular, the ZI projections to the superior colliculus are thought to be involved in initiating orientative eye and head movements (Schall, 1995; Moschovakis, 1996). These projections arise mainly from the ZIv and are topographically organized (see above). In cats, distinct eye and head orientating movements occur when the ZI is stimulated (Kaelber and Smith, 1979). Other

Posture and locomotion

Functional studies have shown that electrical or chemical stimulation of the ZI generates locomotor activity and particular limbic-related movements, such as those associated with defense orientation (Mogenson et al., 1985; Milner and Mogenson, 1988; Murer and Pazo, 1993; Supko et al., 1991, 1992; Pèrier et al., 2002). Further, lesions of the ZI render male rats unable to sexually mount females, while not affecting their sexual motivation. The ZI is thought important in the execution of the

Summary

The ZI has been associated with four major functions. In some instances, authors have reported that stimulation or lesion of a given ZI region or sector produces distinct changes in a particular function. For example, stimulation or lesion to the rostral regions of the ZI, and not others, will produce changes in ingestive activity (Tonelli and Chiaraviglio, 1993) or hormonal release (Sanghera et al., 1991), while stimulation or lesion to caudal regions of the ZI will generate changes in posture

Speculating on a global incertal function: A sensory link to arousal, attention, visceral and locomotion function?

Although there have been many studies exploring firstly, the details of ZI structure and connectivity, or secondly, a particular function associated with ZI, there have been few studies that have considered the overall function and significance of the zone. Indeed, is there is a global role for the ZI, one that involves all the many cell types and links the diverse functions together? To this end, it is worth summarizing the important features of ZI structure and function discussed thus far:

Clinical perspective: The potential importance of the ZI in Parkinson disease

There is an ever growing body of work, stretching back nearly 40 years, indicating that the ZI is important in several clinical settings. After electrical or chemical (cholinergic agonists) stimulation, rats are more likely to develop a generalized seizure than after such stimulations of other brain regions (Gioanni et al., 1991; Brudzynski et al., 1995). This feature reflects the extensive connections that the ZI has with many forebrain and brainstem regions, manifesting in the spread of

Summary

The ZI is associated with the constellation of functions that are potentially disrupted in Parkinson disease, indicating that the region may form a hopeful and exciting prospect for future drug and/or surgical treatment of this disease. It remains to be determined if stimulation of cells in different sectors of the ZI generates different clinical symptoms. This would require a detailed postmortem histological analysis of the electrode location in the ZI sector(s), relating this location to the

Conclusions

There is so much that remains uncertain regarding this “zone of uncertainty” located deep in the brain. However, some promising insights have been amassed since Forel's (1877) first description all those years ago. Many authors have described distinct ZI functions, from arousal to attention and from visceral control to posture–locomotion. Collectively, the ZI may serve to integrate diverse sensory inputs and provide a link to appropriate arousal, attention, visceral and posture/locomotion

Acknowledgments

I thank my wonderful students Brian Power, Christian Kolmac, Claire Heise, Fiona Reardon, Victoria Shaw and Lilijana Mikuletic, for providing much of the data with which to consider. Sharon Spana provided invaluable technical help throughout. I'm thankful to Bjorn Merker who provided the inspiration to write this review. Ray Guillery and Gary Baker were kind enough to read early versions of this manuscript and provide insightful and thought-provoking comments. I am ever grateful to the Tenix

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ReviewSome certainty for the “zone of uncertainty”? Exploring the function of the zona incerta

Abstract

Section snippets

Cytoarchitecture

Summary

Chemoarchitecture

Summary

Connections

Summary

Functions

Visceral activity

Arousal

Attention

Posture and locomotion

Summary

Speculating on a global incertal function: A sensory link to arousal, attention, visceral and locomotion function?

Clinical perspective: The potential importance of the ZI in Parkinson disease

Summary

Conclusions

Acknowledgments

Brain Res

Neurosci Lett

Brain Res

Prog Neurobiol

Neuroscience

Behavioural evidence. Brain Res

Behav Brain Res

Brain Res

Neuroscience

Epilepsy Res

Brain Res

Exp Neurol

Brain Res

Brain Res Bull

Neurosci Lett

Neurosci Lett

Lancet

Neuroscience

Brain Res

Neurosci Res

Brain Res

Curr Opin Neurobiol

Brain Res Bull

J Clin Neurosci

Brain Res

Neuroscience

Exp Neurol

Brain Res

Neurosci Lett

Neuroscience

The zona incerta. Brain Res

Brain Res Bull

Neuroscience

Brain Res

Brain Res

A study of tremor in multiple sclerosis

Brain

Projections from the lateral and interposed cerebellar nuclei to the thalamus of the rat: a light and electron microscopic study using single and double anterograde labelling

J Comp Neurol

Projections from the cerebellar interposed and dorsal column nuclei to the thalamus in the rat: a double anterograde labelling study

J Comp Neurol

Selective GABAergic innervation of thalamic nuclei from zona incerta

J Neurosci

Mechanisms of deep brain stimulation

Mov Dis

Pathophysiology of Parkinson disease: from clinical neurology to basic neuroscience and back

Mov Dis

Are there connections between the thalamic reticular nucleus and the brainstem reticular formation?

J Comp Neurol

Hypocretin/orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems

J Comp Neurol

Cholinergic mechanisms in generalised seizures: importance of the zona incerta

Can J Neurol Sci

Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area

J Comp Neurol

Characterization of CART neurons in the rat and human hypothalamus

J Comp Neurol

Untersuchungen üb r die Haubenr gion und ihre ob r n V rknüpfungen im Gehirne des Menschen und einiger Säugethier

Arch Psychiat Nerv Nkr

The diencephalon of albino rat: studies on the brain of the rat

Review
Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta