Gray Matter

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Brain tissue can be broadly categorized as gray matter, white matter, or cerebrovascular fluid. These different tissue types are discriminated by MRI and define the anatomical boundaries of most brain structures. Gray matter generally consists of cell bodies and white matter of myelinated axon fibers. The gray matter changes during adolescence are presented for different regions of the cerebral cortex as well as for the subcortical basal ganglia, amygdala, and hippocampus.

A. Cortical Subdivisions

The brain is often divided into four lobes with functionally distinct properties: the frontal, temporal, parietal, and occipital lobes.

1. Frontal Gray Matter

The functions of the frontal lobe include planning, organizing, strategizing, as well as initiating, shifting, and sustaining attention. It is sometimes referred to as the "executive" of the brain. As seen in Fig. 2, frontal gray matter increases throughout childhood, peaks at 11 years in girls and 12 years in boys, and then declines throughout adolescence. The peaks correspond to the onset of puberty, although a direct relationship between hormonal changes of puberty and this process has yet to be established. The thickening of cortical gray matter is thought not to reflect an increase in the number of neurons but to be caused by an increase in the number and thickness of branches and connections on the dendrites and axons of existing neurons, a process called arborization. Following this peak of arborization is a pruning process whereby the number of branches and connections are selectively cut back.

Figure 2 Predicted size with 95% confidence intervals for cortical gray matter in frontal, parietal, temporal, and occipital lobes for 243 scans from 89 males and 56 females, ages 4-22 years. The arrows indicate peaks of the curves (reproduced with permission from J. N. Giedd, et al., 1999, Brain development during childhood adolescence. Nat. Neurosci. 2, 861-863).

Figure 2 Predicted size with 95% confidence intervals for cortical gray matter in frontal, parietal, temporal, and occipital lobes for 243 scans from 89 males and 56 females, ages 4-22 years. The arrows indicate peaks of the curves (reproduced with permission from J. N. Giedd, et al., 1999, Brain development during childhood adolescence. Nat. Neurosci. 2, 861-863).

2. Parietal Gray Matter

The parietal lobes are primarily responsible for receiving and processing sensory input such as touch, pressure, heat, cold, and pain. The parietal lobes are also involved in the perception of body awareness and the construction of a spatial coordinate system (mental map) to represent the world around us. Individuals with damage to the right parietal lobe often show striking abnormalities in body image and spatial relations, such as failing to attend to part of the body or space (contralateral neglect). Patients with damage to the left parietal lobe often experience difficulty with writing (agraphia), an inability to recognize familiar objects (agnosia), and language disorders (aphasia). Bilateral damage can lead to problems with visual attention and motor abilities. As with the frontal gray matter, parietal gray matter increases during childhood and decreases during adolescence, peaking at 10.2 years in girls and 11.8 years in boys (Fig. 2).

3. Temporal Gray Matter

The temporal lobes subserve functions of language, emotion, and memory. As opposed to the frontal and parietal gray matter, the temporal gray matter does not peak until age 16.7 years in girls and 16.5 years in boys (Fig. 2). Electroencephalographic studies of adolescents and young adults also indicate ongoing maturation of the temporal lobes throughout the second decade of life.

4. Occipital Gray Matter

The occipital lobes are involved in visual information processing and object recognition. The gray matter in the occipital lobes continues to increase during childhood and adolescence (Fig. 2).

B. Subcortical Divisions 1. Basal Ganglia

The basal ganglia are composed of the caudate nucleus, putamen, globus pallidus, subthalamic nucleus, and substantia nigra. These structures are well-known to influence movement and muscle tone as indicated by their dysfunction in Parkinson's and Huntington's disease, but they are also integral components of circuits mediating higher cognitive functions, attention, and affective states. Of the basal ganglia components, only the caudate, putamen, and globus pallidus are large enough to be readily quantifiable by MRI. Like frontal and parietal cortical gray matter, the basal ganglia generally decrease in volume during the teen years.

2. Amygdala/Hippocampus

The amygdala and the hippocampus are adjacent gray matter structures in the medial temporal lobe. The amygdala is an almond-shaped structure that plays a key role in the brain's integration of emotional meaning with perception and experience. It coordinates the actions of the autonomic and endocrine systems and prompts release of adrenaline and other excitatory hormones into the bloodstream. The amygdala is involved in producing and responding to nonverbal signs of anger, avoidance, defensiveness, and fear. The amygdala has been implicated in emotional dysregula-tion, aggressive behavior, and psychiatric illnesses such as depression. It has also been shown to play an important role in the formation of emotional memory and in temporal lobe epilepsy.

The hippocampus is a horseshoe-shaped region that is involved in short-term memory storage and retrieval. Human capacity for these functions undergoes marked changes from ages 4 to 18 years. However, the relationships between changes in these abilities and changes in brain morphology are not well understood. New memories are kept in the hippocampus before being transferred to the cerebral cortex for permanent storage. This may explain why people with brain damage to their hippocampal region retain previous memories of faces and places, which are stored in the cortex, but have difficulty forming new short-term memories. The hippocampus is also implicated in the learning and remembering of space (spatial orientation). Animal studies show that damage to the hippocampus results in the inability to navigate through familiar areas. In humans, hippocampal damage results in a failure to remember spatial layouts or landmarks. Following stroke damage to the para-hippocampus, patients lose the ability to learn new routes or to travel familiar routes.

During adolescence the size of the amygdala increases sharply for males and less sharply for females. In contrast to the amygdala, the hippocampus increases more robustly in adolescent females. These sex-specific maturational patterns are consistent with nonhuman primate studies that have found a predominance of androgen receptors in the amygdala and a predominance of estrogenic receptors in the hippocampus.

Other lines of evidence also support the influence of estrogen on the hippocampus. Female rats that have had their ovaries removed have a lower density of dendritic spines and decreased fiber outgrowth in the hippocampus, which can be alleviated with hormone replacement. In humans, smaller hippocampi have been reported in women with gonadal hypoplasia, and a recent MRI study of 20 young adults found relatively larger hippocampal volumes in females.

In addition to receptors for gonadal steroids, the hippocampus and amygdala are rich in receptors for adrenal steroids, thyroid hormone, and nerve growth factor. In addition to direct effects on hippo-campal development, estrogen may influence development by blocking neurodegenerative effects of glucocorticoids.

The intricacy of various neurochemical systems and the diversity of afferent and efferent connections to the many distinct nuclei of most brain structures make straightforward relationships between volumes of a single structure and performance on a particular cognitive task uncommon. One of the rare exceptions to this rule is the relationship between hippocampal size and memory function. Birds that store food need better memory than their non-food-storing counterparts and correspondingly have larger hippocampi. Likewise, male polygamous prairie voles travel far and wide in search of mates and have significantly larger hippocampi and perform better on laboratory measures of spatial ability than their female counterparts. In the monogamous vole species, which do not show male-female differences in spatial ability, no sexual dimorphism of hippocampal size is seen. Correlations between memory for stories and left hippocampal volume in humans have also been noted.

Anomalies of temporal lobe and medial temporal lobe structures have been reported for a variety of psychiatric disorders, including affective disorders, autism, and, most consistently, schizophrenia, which is increasingly understood as a neurodevelop-mental disorder. These disorders have marked sex differences in age of onset, symptomatology, and risk factors. The sex-specific maturational differences may have relevance to the expression of these disorders.

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