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Decrements in Volume of Anterior Ventromedial Temporal Lobe and Olfactory Dysfunction in Schizophrenia

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Decrements in Volume of Anterior Ventromedial Temporal Lobe and Olfactory Dysfunction in Schizophrenia ORIGINAL ARTICLE Decrements in Volume of Anterior Ventromedial Temporal Lobe and Olfactory Dysfunction in Schizophrenia Bruce I. Turetsky, MD; Paul J. Moberg, PhD; David R. Roalf, BA; Steven E. Arnold, MD; Raquel E. Gur, MD, PhD Context: Patients with schizophrenia exhibit olfactory ing brain function or olfactory capacity. deficits, but it is unclear whether these represent a spe- cific abnormality. The link between olfactory impair- Main Outcome Measures: Gray matter volumes of ments and regional brain abnormalities has yet to be es- the left and right temporal poles and the perirhinal and tablished. entorhinal cortexes; olfactory threshold detection sen- sitivity and identification test scores; composite indexes Objectives: To determine whether patients with schizo- of verbal and spatial memory ability. phrenia exhibit volumetric deficits in the anterior ven- tromedial temporal lobe, the target for neuronal inputs Results: Patients had reduced volumes, relative to cra- from the olfactory bulb, and whether these are related nial size, in left (P=.003) and right (P=.01) perirhinal to olfactory performance deficits. and left (P=.002) and right (P=.002) entorhinal cor- texes, but not in the temporal pole. Perirhinal, but not Design: A cohort study of patients and healthy control entorhinal, cortical volume decrement was associated with subjects who underwent both 1-mm spoiled-gradient echo decreased olfactory threshold sensitivity. Neither re- magnetic resonance imaging and behavioral tests of ol- gion was associated with impaired memory perfor- faction and memory. mance. Setting: Schizophrenia Research Center at the Univer- Conclusions: Patients with schizophrenia have re- sity of Pennsylvania, Philadelphia. duced cortical volumes in brain regions that receive af- ferents directly from the olfactory bulb. Behavioral ol- Participants: Fifty-two patients with a DSM-IV diag- factory deficits are related to structural brain abnormalities nosis of schizophrenia and 38 healthy control subjects. in these regions. Individuals were excluded for history of head trauma, sig- nificant substance abuse, and medical conditions affect- Arch Gen Psychiatry. 2003;60:1193-1200 HERE IS increasing evi- underlie these impairments.3,4 Whether dence that patients with comparable abnormalities exist in the cor- schizophrenia are im- tical areas that receive neuronal inputs paired in their ability to de- directly from the olfactory bulbs, and tect and identify odors.1 whether these are related to olfactory per- TThese deficits are present early in the dis- formance deficits, are questions that re- ease course and are unrelated to symp- main unanswered. tom severity, medication use,2 or smok- Olfactory processing is mediated by ing. However, it remains unclear whether many of the same medial temporal lobe areas they represent a specific impairment or of the brain that have been implicated in merely reflect the global cognitive impair- schizophrenia. Olfactory afferents travel via ment seen in this disorder. The link be- the olfactory tract to the ipsilateral ante- tween olfactory behavioral impairments rior ventromedial temporal lobe (AVMT), and regional brain abnormalities in schizo- where they synapse with pyramidal cells. phrenia has yet to be established. A re- The bulk of these afferents terminate in the cent finding from our laboratory—that piriform cortex, which is located at the ros- From the Schizophrenia both patients and their healthy first- tral uncus and is thought to be responsible Research Center, Department of degree relatives have reduced olfactory for initial olfactory perception. Some fi- Psychiatry, University of bulb volumes—would suggest that struc- bers terminate posteriorly in the entorhi- Pennsylvania, Philadelphia. tural abnormalities of the olfactory system nal cortex (EC), the gateway to the hippo- (REPRINTED) ARCH GEN PSYCHIATRY/ VOL 60, DEC 2003 WWW.ARCHGENPSYCHIATRY.COM 1193 ©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 memory impairment. In contrast to the large number of Table 1. Patient Clinical Measures* studies examining the hippocampus and amygdala, only 13 studies13,17-28 examined the adjacent parahippocampal Characteristic Men Women gyrus, with 8 (62%) reporting reductions of this cortical Age, y 28.5 (7.2) 36.3 (9.3)† gray matter area. Only 2 studies29,30 examined the EC, de- Age at onset, y 20.2 (5.5) 28.0 (9.9)† spite its role as a critical relay between the hippocampus Duration of illness, y 8.2 (7.0) 7.6 (6.7) 31 Յ and associational cortexes. One of these found bilateral Illness 2 y, No. 10 5 29 Deficit, No. volume reductions in patients, while the other reported 30 Present 4 3 no difference. Hence, it is still unclear to what extent Absent 23 22 AVMT cortical gray matter is reduced in schizophrenia. No Medicated, No. studies, to our knowledge, have looked specifically at the Yes 19 18 cortical regions responsible for olfactory processing and their No 8 7 relationship to olfactory performance. Perhaps one rea- Brief Psychiatric Rating Scale score 35.2 (16.3) 32.8 (15.9) son for the relative dearth of such investigations is the prob- Negative Symptom Scale score Total (items 1-22) 30.0 (24.4) 22.8 (17.1) lem of selecting appropriate MRI landmarks to guide region- Affective Flattening (1-8) 9.1 (8.0) 6.8 (6.2) of-interest (ROI) identification in this area. Boundaries Alogia (9-13) 3.6 (5.1) 2.4 (2.8) between AVMT subregions are based on cytoarchitectural Avolition (14-17) 6.1 (5.3) 2.9 (5.0)‡ distinctions, rather than gross anatomic features. Anhedonia (18-22) 9.8 (6.4) 9.1 (6.8) In this investigation, we applied volumetric MRI Attention (23-25) 2.3 (3.6) 1.4 (2.6) methods to quantify the cortical gray matter volumes of Positive Symptom Scale score Total (items 1-34) 19.2 (17.0) 15.0 (16.4) cytoarchitecturally distinct areas of the AVMT in a large Hallucinations (1-7) 6.2 (6.6) 5.4 (5.6) sample of patients and healthy control subjects. We used Delusions (8-20) 9.5 (8.8) 7.8 (8.9) transitional landmarks derived from histologic analysis5 Bizarre Behavior (21-25) 0.6 (1.5) 0.5 (1.6) to parse the region into discrete TP, PC, and EC. Par- Formal Thought Disorder (26-34) 2.8 (6.2) 1.3 (3.5) ticipants were assessed on olfactory and memory perfor- mance to investigate the relationship between cortical vol- *Data are mean (SD) unless otherwise indicated. †Difference between men and women, P = .001. ume abnormalities and behavior. ‡Difference between men and women, P = .03. METHODS campus. Piriform cortex and EC also connect to the PARTICIPANTS amygdala, thereby providing a neuroanatomic basis for the linkage of olfaction to emotion and memory, 2 processes The sample consisted of 52 patients (27 men, 25 women) with known to be impaired in schizophrenia. Cytoarchitectur- a DSM-IV diagnosis of schizophrenia and 38 healthy volun- ally, the AVMT may be subdivided into temporopolar cor- teers (21 men, 17 women). Patient age ranged from 19 to 53 tex (TP) (Brodmann area 38), perirhinal cortex (PC) (Brod- years (mean±SD, 32.3±9.1 years); healthy control age ranged mann areas 35 and 36), and EC (Brodmann area 28),5 with from 18 to 56 years (mean±SD, 28.2±9.4 years). This repre- sented a small but significant group difference (t88=2.07, P=.04). the piriform cortex included as part of the PC. While the There was also a difference in smoking habits: 5 of 38 controls latter 2, which are considered to be part of the limbic cor- ␹2 Ͻ and 19 of 52 patients were active smokers ( 1=6.14, P .05). tex, have been implicated in olfaction and memory, the TP Mean numbers of packs per day were 0.13±0.30 for controls is generally considered to be developmentally and func- and 0.38±0.51 for patients (t87=2.73, P=.008). There was no tionally distinct. Although it connects to the amygdala, hip- difference between the groups in sex distribution. pocampus, and basal forebrain, it does not receive direct Patients were consecutively referred from both outpa- olfactory afferents. tient and inpatient settings and received medical, neurologic, and psychiatric evaluations, including the Structured Clinical Previous examinations of medial temporal lobe struc- 32,33 tures in schizophrenia, using volumetric magnetic reso- Interview for DSM-III-R–Patient Version. To ensure diag- nance imaging (MRI) techniques, have focused on the amyg- nostic accuracy, they were clinically reassessed at 6-month in- tervals after intake. There was no history of any disorder or event dala-hippocampal complex, with few studies considering other than schizophrenia that could potentially affect brain func- the surrounding cortical areas that mediate olfaction. The tion. All patients who met inclusion criteria and were willing principal motivation for emphasizing these 2 subcortical and able to provide informed consent were included. Healthy structures has been their link to memory and emotion pro- volunteers were recruited by newspaper advertisement and un- cessing. Memory impairments are extremely robust and se- derwent medical, neurologic, and psychiatric (Structured Clini- lective trait abnormalities in schizophrenia6,7; emotion pro- cal Interview for DSM-III-R–Nonpatient Version) evalua- cessing disturbances are gaining new prominence.8-11 In a tion.34,35 They were excluded for any history of Axis I psychiatric recent review of the literature, Shenton and colleagues12 illness; Axis II diagnosis of schizotypal, schizoid, or paranoid identified 34 (71%) of 48 studies that reported significant personality disorder; family history of psychosis; or any medi- volume reductions in the amygdala and/or hippocampus cal condition or occurrence, including substance abuse, that could compromise brain function. Informed consent was ob- in patients. Despite the role of the hippocampus in memory tained from all participants at the time of enrollment.
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