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Olfactory dysfunction in patients with head trauma.

BACKGROUND: The ability to smell is commonly altered by head trauma (HT). However, the nature, prevalence, prognosis, and etiology of such alterations are poorly understood. OBJECTIVES: To quantitatively determine the degree of olfactory function in patients with HT-related chemosensory complaints and to examine the influences of age, sex, HT severity, time since HT, and other variables on such function. Also, to use quantitative magnetic resonance imaging (MRI) to establish whether and to what degree damage to the olfactory bulbs and tracts, frontal lobes, and temporal lobes occurs. PATIENTS AND METHODS: Two hundred sixty-eight patients with HT from the University of Pennsylvania Smell and Taste Center, Philadelphia, were administered a quantitative odor identification test, a depression inventory, and a medical history questionnaire; 66 were retested after individual test-retest periods ranging from 1 month to 13 years. The volume of olfactory-related brain structures was determined in 15 patients and 15 controls using MRI. RESULTS: One hundred seventy-nine patients (66.8%) had anosmia, 55 (20.5%) had microsmia, and 34 (12.7%) had normosmia. Frontal impacts produced less dysfunction than back or side impacts. Of the 66 retested patients, 24 (36%) improved slightly, 30 (45%) had no change, and 12 (18%) worsened; only 3 patients, none of whom initially had anosmia, regained normal olfactory function. Trauma severity was related to olfactory test scores in patients with microsmia. Parosmia prevalence decreased from 41.1% to 15.4% over an 8-year posttrauma period. Olfactory bulb and tract volumes of male, but not female, patients with HT were greatly reduced relative to volumes of controls. CONCLUSIONS: Patients complaining of HT-related olfactory dysfunction typically have anosmia and rarely regain normal olfactory ability, parosmia prevalence decreases over time in such patients, and damage to olfaction-related brain structures can be observed in most such patients using an appropriate MRI protocol.

Adult↗

Obesity as a risk factor for primary spontaneous rhinoliquorrhea.

OBJECTIVE: To determine whether obesity is a potential risk factor of primary spontaneous cerebrospinal fluid rhinorrhea (CSFR). DESIGN: Retrospective study. SETTING: University hospital. PATIENTS AND METHODS: The clinical data of 79 patients diagnosed with CSFR who had been treated at our hospital between 1991 and 2001 were assessed. The data of 61 (77%) of 79 cases were complete and could be used for this study. Patients were segregated according to the cause of their CSFR: 21 (34%) due to head trauma, 14 (23%) due to previous surgery, 7 (11%) due to congenital malformation, and 2 (3%) due to tumor adjacent to the anterior cranial fossa. Of the 61 subjects, 17 (28%) had CSFR without any detectable reason. This group was therefore designated as primary spontaneous CSFR. The body mass indexes (BMIs) of all patients were compared and statistically evaluated. RESULTS: The mean BMI (calculated as weight in kilograms divided by the square of height in meters) of the 17 patients with primary spontaneous CSFR was 34.87, which was significantly higher (P<.001) than the mean BMI of the other 44 patients (28.53). The mean BMI of the group of patients with CSFR due to previous surgery or trauma was significantly lower than the BMI of the group with primary spontaneous CSFR (P<.003), whereas in relation to the group afflicted with tumors and malformations, only a tendency (P<.28) was found. CONCLUSION: Our data suggest that obese patients are at an increased risk to develop primary spontaneous CSFR.

Adolescent↗

Olfactory sarcoidosis. Report of five cases and review of the literature.

Changes in the olfactory system in five patients with sarcoidosis were studied by clinical and histopathological examination. Every patient studied had hypogeusia and/or hyposmia as measured by psychophysical testing. In two patients who died with this disease, the olfactory bulbs and tracts were involved by granulomatous infiltration. Two other patients showed granulomas and chronic inflammation in nasal biopsy specimens. The fifth patient was studied only clinically. Changes in olfactory and gustatory acuity are rarely searched for in patients with sarcoidosis, but they may be important indicators of major and later irreversible damage to the CNS. If diminished olfaction is established in suspect patients, nasal biopsy and examination of the CNS should be performed to confirm the presence of active sarcoidosis. Appropriate therapy may prevent damage to the patient's sensory capabilities and CNS function.

Adolescent↗

Subarachnoid space of the CNS, nasal mucosa, and lymphatic system.

We have briefly reviewed the literature pertaining to the movement of tracer molecules and infectious organisms within the olfactory nerve. There is a body of evidence indicating that tracers placed in the CSF will quickly move via the olfactory nerve to the nasal mucosa and then to the cervical lymph nodes. Organic and inorganic tracer materials and organisms as diverse as viruses, a bacillus, and an amoeba, when placed in the nasal cavity, have been shown to move from the nasal mucosa via the olfactory nerve to the olfactory bulb and the CSF. We think that a portion of the data on tracer movement is due to incorporation of tracer materials and organisms into the axoplasm of the olfactory neurons with subsequent anterograde or retrograde axoplasmic transport. However, some of the movement of tracers may occur within the olfactory perineural space. This space may be continuous with a subarachnoid extension that surrounds the olfactory nerve as it penetrates the cribriform plate. To our knowledge, no one has yet followed the perineural space to determine if it is continuous from olfactory receptor to olfactory bulb. The consideration of this space and its role is the main reason for this review.

Animals↗

Magnetic resonance imaging of the olfactory apparatus.

The magnetic resonance imaging visualization of the olfactory apparatus is reported in this article. We used a superconductor-type magnetic resonance device (Siemens Magnetom H15 (1.5 T) with a surface coil. The subjects were patients with posttraumatic anosmia. The olfactory bulbs were clearly visualized in the frontal plane magnetic resonance images, the olfactory bulbs and the foramina of the cribriform plate were visualized in the sagittal section, and the olfactory bulbs, tracts, and other structures were visualized in the coronal sections. The olfactory nerves could not be seen.

Brain Diseases↗

Differences and similarities in insular and temporal pole MRI gray matter volume abnormalities in first-episode schizophrenia and affective psychosis.

CONTEXT: Whether psychoses associated with schizophrenia and affective disorder represent manifestations of different disorders or the same disorder is an important but unresolved question in psychiatry. Results of previous volumetric magnetic resonance imaging investigations indicate that gray matter volume reductions in neocortical regions may be specific to schizophrenia. OBJECTIVE: To simultaneously evaluate multiple olfactocentric paralimbic regions, which play crucial roles in human emotion and motivation, in first-episode patients with schizophrenia and affective psychosis. DESIGN: A cross-sectional study using high-spatial resolution magnetic resonance imaging in patients with schizophrenia and affective psychosis at their first hospitalization. SETTING: Inpatient units at a private psychiatric hospital. PARTICIPANTS: Fifty-three first-episode patients, 27 with schizophrenia and 26 with affective (mainly manic) psychosis, and 29 control subjects. MAIN OUTCOME MEASURES: Using high-spatial resolution magnetic resonance imaging, the gray matter volumes of 2 olfactocentric paralimbic regions of interest, the insular cortex and the temporal pole, were evaluated. RESULTS: A bilateral volume reduction in insular cortex gray matter was specific to first-episode patients with schizophrenia. In contrast, both first-episode psychosis groups showed a volume reduction in left temporal pole gray matter and an absence of normal left-greater-than-right asymmetry. Region of interest correlations showed that only patients with schizophrenia lacked a positive correlation between left temporal pole and left anterior amygdala-hippocampal complex gray matter volumes, whereas both psychosis groups were similar in lacking normal positive correlations between left temporal pole and left anterior superior temporal gyrus gray matter volumes. CONCLUSIONS: These partially different and partially similar patterns of structural abnormalities in olfactocentric paralimbic regions and their associated abnormalities in other temporolimbic regions may be important factors in the differential and common manifestations of the 2 psychoses.

Acute Disease↗

Decrements in volume of anterior ventromedial temporal lobe and olfactory dysfunction in schizophrenia.

CONTEXT: Patients with schizophrenia exhibit olfactory deficits, but it is unclear whether these represent a specific abnormality. The link between olfactory impairments and regional brain abnormalities has yet to be established. OBJECTIVES: To determine whether patients with schizophrenia exhibit volumetric deficits in the anterior ventromedial temporal lobe, the target for neuronal inputs from the olfactory bulb, and whether these are related to olfactory performance deficits. DESIGN: A cohort study of patients and healthy control subjects who underwent both 1-mm spoiled-gradient echo magnetic resonance imaging and behavioral tests of olfaction and memory. SETTING: Schizophrenia Research Center at the University of Pennsylvania, Philadelphia. PARTICIPANTS: Fifty-two patients with a DSM-IV diagnosis of schizophrenia and 38 healthy control subjects. Individuals were excluded for history of head trauma, significant substance abuse, and medical conditions affecting brain function or olfactory capacity. MAIN OUTCOME MEASURES: Gray matter volumes of the left and right temporal poles and the perirhinal and entorhinal cortexes; olfactory threshold detection sensitivity and identification test scores; composite indexes of verbal and spatial memory ability. RESULTS: Patients had reduced volumes, relative to cranial size, in left (P =.003) and right (P =.01) perirhinal and left (P =.002) and right (P =.002) entorhinal cortexes, but not in the temporal pole. Perirhinal, but not entorhinal, cortical volume decrement was associated with decreased olfactory threshold sensitivity. Neither region was associated with impaired memory performance. CONCLUSIONS: Patients with schizophrenia have reduced cortical volumes in brain regions that receive afferents directly from the olfactory bulb. Behavioral olfactory deficits are related to structural brain abnormalities in these regions.

Adolescent↗

Concentration and storage of biotin in the amphibian brain.

Prominent displays of endogenous biotin reactivity can be observed at specific locations in histochemical preparations of the forebrain and midbrain in the northern leopard frog (Rana pipiens) and common American toad (Bufo americanus). At the light microscopic level, the biotin reactivity appears in clusters of darkly stained puncta of either spherical or rodlike shape in the olfactory cortex, nucleus isthmi, and hypothalamus. With the electron microscope, the biotin reactive spheres are identified as neuronal varicosities and synaptic boutons and the rods as short segments of axons. Appropriate controls demonstrate that the punctate biotin-reactive structures are sites of concentration of biotin or a biotin analog in the processes of certain neurons. These data represent the first observation on the selective concentration of a vitamin in vertebrate neurons and suggest that biotin may have specialized functions in anatomically delimited areas of the central nervous system. Localization of the densest concentration of the biotin-reactive puncta in the dorsolateral prominence of the olfactory cortex may have relevance to the functional organization of the olfactory system. The distributions of biotin-reactive puncta were observed in laboratory-housed frogs and in wild toads captured in the summer months but were sparse or absent in batches of commercially obtained frogs examined immediately upon arrival in the laboratory. Systemic administration of biotin or biocytin hydrochloride did not alter the appearance or numbers of the biotin-reactive structures either in newly received or laboratory-housed frogs. These findings suggest that the capacity of the biotin-storage mechanism in the amphibian brain may be set by environmental factors and may be readily saturable from natural dietary or enteric sources.

Animals↗

Distribution of the mRNA for a pituitary adenylate cyclase-activating polypeptide receptor in the rat brain: an in situ hybridization study.

The distribution of the mRNA for a pituitary adenylate cyclase-activating polypeptide (PACAP) receptor (PACAP-R) was examined in the rat brain, and also in the hypophysis and pineal gland, by in situ hybridization with a specific 35S-labeled riboprobe which was generated from a rat PACAP-R cDNA clone. In the brain, expression of PACAP-R mRNA was most prominent in the periglomerular and granule cells of the olfactory bulb, granule cells of the dentate gyrus, supraoptic nucleus, and area postrema. The expression was also intense in the piriform, cingulate, and retrosplenial cortices, pyramidal cells in CA2, non-pyramidal cells in CA1-CA3, neuronal cells in the hilus of the dentate gyrus, lateral septal nucleus, intercalated amygdaloid nucleus, anterodorsal thalamic nucleus, most of the midline and intralaminar thalamic nuclei, many regions of the hypothalamus, dorsal motor nucleus of the vagus nerve, hypoglossal nucleus, and lateral reticular nucleus. No significant expression was detected in the mitral and tufted cells in the olfactory bulb, pyramidal cells in CA1 and CA3, posterior nuclear group of the thalamus, dorsal lateral geniculate nucleus, and Purkinje, Golgi, and granule cells in the cerebellar cortex. Moderate-to-weak expression was further observed in many other regions of the brain. In the cerebellar cortex, presumed Bergmann glia cells showed moderate expression. In the hypophysis, the expression was moderate in the anterior lobe, and weak to moderate in the posterior lobe; no significant expression was observed in the intermediate lobe. In the pineal gland, the expression was very weak, if any. Thus, the expression of PACAP-R was detected not only on neuronal cells but also on some particular glial cells. The present study has shown, for the first time, the exact site of PACAP-R expression in the brain and hypophysis. Although the functional significance of PACAP and PACAP-R in the brain still remains to be clarified, the present results are considered to provide some direction for future functional studies.

Animals↗

GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system.

To help elucidate the role of inhibitory feedback in the genesis of odour-evoked synchronization of neural activity, we investigated the distribution of gamma-aminobutyric acid (GABA)ergic synaptic terminals in the antennal lobes (AL) and mushroom bodies (MB) of the locust olfactory system. Electron-microscopy, intracellular horseradish peroxidase labelling, and immunocytochemistry were combined to assess the distribution of GABAergic synapses, using established methods (Leitch and Laurent [1993] J. Comp. Neurol. 337:461-470). In the AL, GABA-immunoreactive presynaptic terminals contacted both immunoreactive and immunonegative profiles. Conversely, GABA-immunoreactive profiles received direct input from both reactive and negative terminals. The tract containing the axons of the projection neurons that run from the AL to the MB contained about 830 axons of fairly uniform size, none of which was immunoreactive for GABA. In the calyx of the MB, large immunoreactive terminals contacted very-small-diameter profiles thought to belong to the Kenyon cells (KCs). This was confirmed by combining immunocytochemistry with intracellular HRP-labelling of KCs. KCs were not immunoreactive for GABA. Although some GABAergic contacts were made onto the spiny profiles of KCs, others were made onto their dendritic shafts. Large GABA-immunoreactive profiles were also found to contact large negative profiles that were presynaptic to KC terminals. This suggests that KC dendrites can be both pre- and post-synaptically inhibited in the calyx. The MB pedunculus contained ca. 50,000 tightly packed KC axons, showing conspicuous en passant and often reciprocal synaptic contacts between neighbouring axons. KC axons were immunonegative, but received direct input from, and contacted directly, large immunoreactive profiles running across or along the KC axons. In the alpha- and beta-lobes of the MB, connections similar to those in the pedunculus were seen with two main differences: (1) The density of synaptic profiles was higher, giving on occasion numerous serially connected profiles in a single section; (2) large immunonegative profiles with dense-core vesicles were abundant and were frequently presynaptic to GABAergic processes and to very-small-diameter profiles which possibly belong to KCs. These results are discussed in the context of the known physiological data on olfactory processing in these complex circuits.

Animals↗

Comparison of the expression of a T alpha 1:nlacZ transgene and T alpha 1 alpha-tubulin mRNA in the mature central nervous system.

We have previously demonstrated that one member of the alpha-tubulin multigene family, termed T alpha 1 in rats, is a panneuronal gene that is regulated as a function of neuronal growth and regeneration. Moreover, 1.1 kb of the 5' upstream region from this gene is sufficient to direct expression of a marker gene to growing neurons in transgenic mice. In this report, we have characterized the distribution of the T alpha 1:nlacZ transgene in the mature central nervous system in two lines of transgenic mice and have compared its expression to that of the endogenous T alpha 1 alpha-tubulin mRNA. These results demonstrate that the pattern of expression of the T alpha 1:nlacZ transgene is similar to that of T alpha 1 mRNA, with a few notable differences. Furthermore, expression of the transgene and the mRNA within the mature brain is panneuronal and, in many cases, is highest in those populations of neurons that show some capacity for morphological growth. These results, together with our previous studies on mature regenerating neurons (Gloster et al. [1994] J. Neurosci. 14:7319-7330; Wu et al. [1994] Soc. Neurosci. Abstr. 20:542) suggest that the T alpha 1:nlacZ transgene will provide a useful marker of growth-associated gene expression in the mature nervous system.

Animals↗

Relationship of gonadotropin-releasing hormone (GnRH) neurons to the olfactory system in developing lamprey (Petromyzon marinus).

Gonadotropin releasing-hormone (GnRH) regulates the hypothalamo-pituitary-gonadal axis in vertebrates. The regulation of GnRH is intimately related to information from the olfactory system. Additionally, GnRH neurons are thought to be derived from progenitor cells in medial olfactory placodes. The present experiments were conducted to characterize the earliest development of GnRH neurons in lamprey and to determine their relationship to cells and fibers derived from the olfactory system. Eggs from fertile adult sea lamprey were fertilized in the laboratory, and larvae were maintained for up to 100 days. GnRH neurons were visualized within the lamprey preoptic area and hypothalamus as soon as GnRH was detectable (22 days after fertilization). The number of neurons increased with age through day 100. GnRH neurons were never seen within the olfactory system. The cells and fibers of the olfactory system were identified using the lectin, Grifonia Simplicifolia-1 (GS-1). Overlap between the olfactory and GnRH systems were at the level of fiber projections. GS-1 reactive cells of apparent placodal origin did not enter the region of the preoptic area or hypothalamus that contained GnRH neurons. Recently divided cells were labeled with the thymidine analog, bromodeoxyuridine (BrdU). The positions of BrdU-labeled cells after different survival times suggest a predominant medial-lateral radial neuron migration with a small number in positions suggestive of migration between the olfactory epithelium and the telencephalic lobes. Regardless of survival time, these cells were always found close to their entry point into the brain, suggesting minimal rostral-caudal migration. Based on these results, we hypothesize that GnRH neurons in developing lamprey originate within proliferative zones of the diencephalon and not in the olfactory system. Based on the overlap of olfactory- and GnRH-containing fibers from prolarval stages to metamorphosis, olfactory stimuli may play a major role in the regulation of GnRH secretion in lamprey.

Aging↗

Intrinsic association fiber system of the piriform cortex: a quantitative study based on a cholera toxin B subunit tracing in the rat.

By using retrograde and anterograde transport of the B subunit of cholera toxin (CTb), we examined quantitatively the association fiber systems, i.e., the collaterals of pyramidal cell axons, that reciprocally connect both the rostral and the caudal parts of the piriform cortex (PC). Well-defined CTb injections were obtained in layers Ib or II-III of the rostral and the caudal parts of the PC. Using precision counting, we determined the proportion of cellular profiles in layers II and III that gave rise to association fibers and thus demonstrated a predominance of rostrocaudal fibers over the caudorostral ones. Our data also support a precise laminar organization of the PC in which the rostrocaudal fibers originated mainly from layer II and the caudorostral fibers primarily from layer III. Cholera toxin injections into layer Ib produced a peak of labeled profiles 2 mm from the site, indicating that a large proportion of the association fibers from layer II travel for at least 2 mm and then synapse in layer Ib. At either end of the PC, the association projections with respect to olfactory processing, propagation of the activity within the PC, and the possible role of intrinsic fibers in olfactory memory.

Animals↗

A compartment-based, asymmetric representation of the retina in an induced projection to the olfactory cortex.

Displacing the optic nerve into the telencephalon in adult Rana pipiens induces a projection to olfactory cortex. We have examined the topographic organization of this projection anatomically by injecting a mixture of biotin dextran (BDA) with 3H-amino acids into the affected eye immediately after making cuts across defined sectors of the nerve fiber layer to trace the complementary patterns of anterograde migration of BDA and 3H label in the cut and intact retinal axons, respectively. Fibers from the temporal side of the optic disc terminated in an oblique band along the posterior two-thirds or more of the ectopic projection field. In contrast, fibers arising in the nasal retina terminated in a parallel strip occupying the anterior one-third or less of the field. Varying the location of the cuts within each hemiretina did not reveal any further organization along the nasotemporal or dorsoventral axes of the retina. The retinal location of the cells involved in this projection was further studied with injections of wheat germ agglutinin conjugated to horseradish peroxidase into the olfactory cortex. Ganglion cells labeled by retrograde transport were found throughout the retina, but they were much more numerous on the temporal side, having a mean spatial density 3.7-7.4 times greater in the temporal hemiretina, whereas the overall ganglion cell density (labeled plus unlabeled) was roughly the same in the two halves of the retina. These data provide an example of a permanent projection in which the overall representation of the retina, though nontopological, is polarized in one axis (nasotemporal) and, therefore, compartmentally organized.

Animals↗

Distribution of radial glia in the developing telencephalon of chicks.

Radial glia are known to have a sparse and uneven distribution in the telencephalon of adult birds. The present study utilizes antibodies against vimentin to reveal a more extensive, and more clearly radial, set of radial glia in the chicken telencephalon during the first half of embryogenesis. This initially extensive radial glial fiber system becomes distorted and reduced between 10 and 14 days of incubation. This reduction coincides with the cytoarchitectural differentiation of the telencephalon into its major adult subdivisions. Because developing neurons tend to migrate along radial glial fibers in both birds and mammals, a topological projection of these major subdivisions onto the embryonic ventricular zone along the radial glial fibers suggests hypotheses about lineage relationships that can be tested by subsequent experimental methods. This analysis suggests that the major components of the avian dorsal ventricular ridge, i.e., the ventral hyperstriatum, the neostriatum with its various subdivisions, part of the archistriatum, and probably also the piriform cortex, all derive from overlapping portions of the lateral pallial ventricular zone. Staining with antibodies against neurofilament suggests that this developmental parcellation of the lateral pallial complex is associated with the development of neuronal fiber systems.

Animals↗

Representation of the calyces in the medial and vertical lobes of cockroach mushroom bodies.

Previous studies of honey bee and cockroach mushroom bodies have proposed that afferent terminals and intrinsic neurons (Kenyon cells) in the calyces are arranged according to polar coordinates. It has been suggested that there is a transformation by Kenyon cell axons of the polar arrangements of their dendrites in the calyces to laminar arrangements of their terminals in the lobes. Findings presented here show that cellular organization in the calyx of an evolutionarily basal neopteran, Periplaneta americana, is instead rectilinear, as it is in the lobes. It is shown that each calyx is divided into two halves (hemicalyces), each supplied by its own set of Kenyon cells. Each calyx is separately represented in the medial lobe where the dendritic trees of some efferent neurons receive inputs from one calyx only. Kenyon cell dendrites are arranged as narrow elongated fields, organized as rows in each hemicalyx. Dendritic fields arise from 14 to 16 sheets of Kenyon cell axons stacked on top of each other lining the inner surface of the calyx cup. A sheet consists of approximately 60 small bundles, each containing 5-15 axons that converge from the rim of the calyx to its neck. Each sheet contributes to a pair oflaminae, one dark one pale, called a doublet, that extends through the mushroom body. Dark laminae contain Kenyon cell axons packed with synaptic vesicles. Axons in pale laminae are sparsely equipped with vesicles. By analogy with photoreceptors, and with reference to field potential recordings, it is speculated that dark laminae are continuously active, being modulated by odor stimuli, whereas pale laminae are intermittently activated. Timm's silver staining and immunocytology reveal a second type of longitudinal division of the lobes. Five layers extend through the pedunculus and lobes, each composed of subsets of doublets. Four layers represent zones of afferent endings in the calyces. A fifth (the y layer) represents a specific type of Kenyon cell. It is concluded that the mushroom bodies comprise two independent modular systems, doublets and layers. Developmental studies show that new doublets are added at each instar to layers that are already present early in second instar nymphs. There are profound similarities between the mushroom bodies of Periplaneta, an evolutionarily basal taxon, and those of Drosophila melanogaster and the honey bee.

Animals↗

Formation of antennal lobe and mushroom body neuropils during metamorphosis in the honeybee, apis mellifera.

The projections to the mushroom bodies (mbs) have been clearly described in the brain of adult honeybees (Apis mellifera). Olfactory projection neurons arborize in the lip of the calyceal neuropil, whereas visual projection neurons project to the collar. To study the maturation of this pattern of innervation, as well as the development of uniglomerular projection neurons within the antennal lobes (als), we conducted the following three studies focused on the first four stages of pupal development: mass staining of olfactory projection neurons, single cell labeling of olfactory projection neurons, and simultaneous labeling of olfactory projection neurons and visual projection neurons. Examination of whole-mount preparations with the confocal laser scanning microscope revealed that the olfactory projection neurons achieved their adult arborization pattern within their main output region, the lip of the mb calyces, earlier during development (pupal stage 1) than their dendritic processes within their main input region, the al (pupal stage 2). Simultaneous labeling experiments showed further that the fiber terminals of olfactory projection neurons and visual projection neurons did not overlap but instead occupied their respective projection areas within the mb calyces as early as pupal stage 1. We conclude that selective innervation of different subregions of the calycal neuropil precedes the segregation of glomerular units within the antennal lobe neuropil, and that the Kenyon cells themselves provide a template for the innervation of olfactory and visual projection neurons.

Age Factors↗