The sense of smell plays a crucial role in human behavior and cognition, with the olfactory system engaging brain regions, including the orbitofrontal cortex (OFC), medial temporal lobe, thalamus, and amygdala which also play key roles in behavioral responses and regulation (Sobel et al., 1998; Eslinger et al., 2004; Rolls, 2004). The OFC contains olfactory cortical areas which are particularly important for olfactory identification (OI) and OI testing can serve as a non-invasive measure of its integrity and functioning (Seidman et al., 1992; Kern et al., 2000; Vasterling et al., 2000) given that damage to the OFC has been associated with olfactory dysfunction (OD) (Li et al., 2010; Seubert et al., 2012) as well as behavioral dysregulation and impulsivity (De Guise et al., 2015).

Olfactory dysfunction (OD) is commonly observed in certain neurodegenerative diseases and may occur in the context of neuropsychiatric disorders such as schizophrenia, depression and panic disorder (Ryo et al., 2017; Fóz et al., 2022). Neural pathways for olfactory processing overlap with those important for aspects of executive functioning concentrated in the frontal lobe, and tests of executive function and olfaction have been shown to positively correlate across a broad array of measures, as recently reviewed (Ramaswamy and Schofield, 2022). Indeed, some investigators have suggested that olfactory tests could serve as a rapid screen for cognitive impairment (Jung et al., 2019; Vance et al., 2023).

Traumatic brain injury (TBI) may cause OD, referred to as “post-traumatic olfactory dysfunction” (PTOD) (Howell et al., 2018). PTOD may arise due to damage to the nasal sinuses, peripheral olfactory structures or central, cerebral olfactory structures (Schofield and Doty, 2019). The orbitofrontal and temporal lobes that include principal elements of the olfactory pathways are particularly vulnerable to TBI damage contributing to the association of TBI with OD (Schofield et al., 2014; Arnold et al., 2020; Pellegrino et al., 2021). The intensity and the extent of TBI influence the likelihood of developing PTOD and of its recovery (i.e., less likely when severe) and therefore the presence of OD in the context of a reported past TBI can serve as an indication of possibly greater TBI severity (Konstantinidis et al., 2013; Schofield et al., 2014).

Violent offenders often exhibit impulsivity and aggression and also have high rates of past TBI (Cuomo et al., 2008; Williams et al., 2018); thus it might be anticipated that violent offenders as a group would perform more poorly on olfactory testing than the general population. Although we are not aware of studies that have specifically sought such a finding, several studies offer tangential support for such a hypothesis. Thus, in one study individuals with psychopathic traits, a phenotype overrepresented within offending populations, performed worse than controls on olfactory testing (Mahmut and Stevenson, 2012) and sociopathic behavior (of which impulsive aggression constitutes a form) has been shown to be associated with damage, dysfunction and or relative atrophy of the OFC (Nummenmaa et al., 2021), itself a correlate of olfactory dysfunction, as has been outlined briefly above.

We hypothesized that among a sample of impulsive violent offenders, olfactory performance would be poorer than appropriate population normative scores, on the basis that many such individuals likely manifest behavioral characteristics of OFC dysfunction, in some instances related to past TBI. To the extent that historical indices of TBI severity were available, we also hypothesized that greater severity TBIs would be associated with poorer performance on olfactory testing. Thus, our major objects in this study were, first, to determine if individuals with a violent profile exhibit a distinct olfactory ability compared to the general population and, second, to determine if reported severity of past TBI was reflected in differences in olfactory performance. In previous studies, a number of other factors, including impulsivity, general intelligence and the extent of an individual’s social network, have been shown to be associated with olfactory performance (Danthiir et al., 2001; Meyer et al., 2010; Zou et al., 2016; Herman et al., 2018). Thus our third specific objective was to determine if we could replicate these findings. We hoped that by undertaking this study we could add both to the growing general literature concerning the neuropsychiatric correlates of olfactory test performance, as well as the specific literature relating to evaluations and prediction, pertinent to offending and the criminal justice system.

All data for the present analyses were obtained from participants at the baseline of the study, before any exposure to sertraline. Data from 693 individuals was used for the initial analysis, however, for a variety of reasons, including difficulties relating to the COVID epidemic, 208 did not undergo OI testing. Differences between those who did not and the 485 who did get SS were few: the former were somewhat more impulsive, more likely to have been suspended, had more suicidality, and reported more alcohol and substance use (Supplementary Tables 1, 2).

In the 5 years prior to their recruitment to the study, participant offending histories comprised the following: 98% had been found guilty of any offense and 48% had been in custody; 63% had committed an act of domestic violence and 58% an act of non-domestic violence; 51% had committed property damage and 87% had committed other offenses not included in the above categories of offending.

When SS scores of the 485 were compared against normative data for age, the offender sample as a group demonstrated significantly lower olfactory performance in the age category 21–30, 31–40, and 41–50 (Oleszkiewicz et al., 2019; Table 1).

Table 2 presents the demographic features of the SS sample stratified by hyposmia and normal olfaction. About 67% of the study participants were between 18 to 35 years old. Most (85%) were of non-Aboriginal descent and living with their parents, partners, or relatives (86%). Half were never married and 45% of participants with hyposmia had been unemployed for at least 6 months.

Participants of this study were all impulsive men who had committed violent offenses. There were very high rates of TBI, personality disorder, suicidality and substance abuse. The main findings with respect to olfaction were, as we hypothesized, that the sample overall had lower mean SS scores compared to the general population norms, with 16% of participants classified as having hyposmia. Our second hypothesis was also supported: greater TBI severity on self-report (i.e., LOC > 30 min) was associated with poorer scores on olfactory testing, both in univariate and in multivariate analyses adjusted for other factors. With respect to our third objective, impulsivity scores were (inversely) associated with olfactory performance in group comparisons, and univariate and multivariate analyses and we found associations between olfactory performance and a cognitive screen (the WIAT), and differences in grouped comparisons (hyposmia vs. normosmia) for depressive symptoms, anger, and childhood sexual abuse.

The finding that the mean performance on the olfactory identification ability of the sample was lower than population norms has multiple possible explanations. While it is well-established that olfactory dysfunction may arise as a consequence of injury or disease there is now evidence that cognitive test performance is intrinsically associated with olfaction, leading to positive correlations of cognitive testing with olfactory performance in the presumptive absence of underlying pathology (Danthiir et al., 2001; Meyer et al., 2010; Dahmani et al., 2018; Gellrich et al., 2021). Within the present sample, the WIAT score, an index of verbal ability, was significantly associated with the SS score in univariate and multivariate analyses. As a group, the individuals in our study clearly had problems engaging with school, with multiple suspensions and expulsions, and about a third left school without any qualification suggesting that as a group they might not perform well on cognitive testing. Surprisingly, however, the mean score of the reading test item from the WIAT II (Wechsler, 2001) for the sample was within the “average” range. This test is very similar in basic design to the National Adult Reading Test (Nelson and Willison, 1991) which is more widely used as a test resistant to the effects of brain damage to estimate “premorbid intelligence.” The precision of the reading test component from the WIAT II for estimation of “intelligence” is less well established. Thus, while we might have anticipated lower than average cognitive ability as a measure “explaining” lower than normative performance on OI, we do not have evidence to support that. On the other hand, the sample was selected based on the criteria of high BIS-11 score and previous studies have shown an association of low olfaction with impulsivity, a finding with which our findings are clearly consistent (Dileo et al., 2008; Herman et al., 2018; Brassard and Joyal, 2022). Thus, lower-than-expected olfactory performance in our sample, based on existing norms, might be explained partly by their high impulsivity, a behavioral characteristic influenced by OFC function/dysfunction. Whether the impulsivity itself, or underlying abnormalities of OFC suggested by it, explain the low olfactory scores is a matter we will consider more later.

The high prevalence of past TBI within the sample is also relevant to the low mean scores on the SS within the entire sample. Our analyses demonstrated a “dose effect,” namely an association of olfactory performance (and prevalence of hyposmia) with the severity of TBI based upon self-reported duration of LOC (Tables 3, 4, 5). Such findings are consistent with previous research linking TBI and olfactory dysfunction with a greater likelihood of olfactory impairment after more severe TBI (Ogawa and Rutka, 1999; Callahan and Hinkebein, 2002; Green et al., 2003; Sigurdardottir et al., 2010, 2016; Welge-Lussen et al., 2012; Gudziol et al., 2014; Schofield et al., 2014; Howell et al., 2018; Singh et al., 2018; Schneider et al., 2022). As indicated earlier, multiple mechanisms may account for the olfactory changes following TBI, including damage to frontal cortical structures such as OFC. OFC is a structure important both for olfaction identification and behavioral regulation; impulsivity, and most of the remaining correlates of olfactory performance that we found, can be considered as potentially reflective of those shared structural/functional affiliations.

Study criteria for the ReINVEST were designed to recruit men with a history of impulsive violence. The neurobiological basis for this syndrome is recognized to include an acquired heightened “threat response,” often during neurodevelopment, mediated by circuits within the brain which include the amygdala and the prefrontal cortex, including the OFC (Bertsch et al., 2020). Of the extrinsic factors known to confer risk for reactive (impulsive) aggression, adverse childhood events (ACE) (including sexual abuse) are especially toxic (Tomoda et al., 2009; Hanson et al., 2010; Van Harmelen et al., 2010; McCrory et al., 2011) and 31% of participants in our study reported such childhood sexual abuse. Reductions in OFC volumes have been consistently reported in the context of ACE and have also been shown in studies of violent individuals (Yang and Raine, 2010; Begemann et al., 2023). Other studies have shown positive correlations between OFC volume and olfactory identification scores (Seubert et al., 2012). Thus, multiple mechanisms—whether neurodevelopmental or due to damage or disease—that affect areas of OFC that engage both olfactory and behavioral regulatory networks may account for the associations we have identified.

An inverse association of olfaction and impulsivity has been found in a range of other settings, not necessarily violence-related. Thus, a previous study found olfactory identification deficits in war veterans with post-traumatic stress disorder (PTSD), which were also significant predictors of aggression (Dileo et al., 2008) and in a study of healthy volunteers, the two variables were associated (Herman et al., 2018). Given the known OFC affiliations of olfaction and impulsivity, and the susceptibility of this structure to damage in the context of TBI, common in offenders, it is unsurprising that we identified associations between those three variables (depicted in Table 5 and in regression analyses Tables 6, 7). Table 6 serves as an aid to conceptualizing the complex associations between impulsivity, TBI and offending, with olfactory performance serving as a proxy for OFC functioning. Inspection of that table indicates that more severe TBIs were associated with worse olfaction but without any difference in impulsivity, relative to milder TBI. One explanation for this dissociation of impulsivity with olfaction is that, in the context of TBI, olfactory impairments can be caused by sinus or peripheral olfactory pathway damage such as axonal shearing of olfactory fibers at cribriform plate that does not have direct behavioral/cognitive consequences. On the other hand, men who reported three or more TBIs were more impulsive (without having poorer olfaction), consistent with the notion that impulsivity is a risk factor for any and recurrent TBI. Neurobehavioral disturbances, such as high impulsivity, may exacerbate antisocial behavior, increasing the risk of criminality and recidivism and leading to TBI (Lane et al., 2017). Conversely, TBI can also lead to impulsivity and executive disorders, further emphasizing the complex interplay between these factors (Rochat et al., 2009; Kocka and Gagnon, 2014). Here, olfactory deficits might be present both before TBI—as correlates of OFC changes related to increased impulsivity—or after TBI—because of brain injury.

A further example of an association in our data that might reflect the measurement of function in topologically overlapping neural pathways is the positive association of SS score with social support scores suggesting that better olfactory function may be associated with stronger social support networks. The findings in relation to this variable were relatively weak—they were not apparent in the comparison of hyposmic and normosmic participants, and while significant in univariate analyses did not retain significance in the multivariate analyses (although p = 0.068 in the normal olfaction group). Previous studies indicate the importance of the frontal lobe, including OFC, for social functioning and an association of olfactory function (sensitivity) with measures of social connectedness has been demonstrated (Zou et al., 2016; Kwak et al., 2018). Social support has been identified as a protective factor against criminal behavior, highlighting the importance of understanding this relationship in offender populations (Cullen, 1994; Spohr et al., 2016). The finding that depressive symptoms were more frequent in the normosmic population, relative to hyosmics, was unexpected and contrary to previous research showing a link between olfactory dysfunction and depression (Naudin et al., 2012; Croy et al., 2014; Eliyan et al., 2020; Vance et al., 2023). That the symptoms were at most mild and we excluded individuals with active depression may partly explain this finding.

Our findings suggest that impaired olfaction, and therefore OI, may also serve as a marker for underlying neurobiological changes that contribute to behavioral disturbances, such as violence or those seen in PTSD or other anxiety-related disorders. The primary olfactory cortex and extended olfactory circuit, which are responsible for the neurobiology of olfaction, also share neural pathways and structures with the anxiety-fear system (Cortese et al., 2017). Finally, in line with our results, OI can serve as a proxy for TBI severity, given that TBI-related brain changes are also found in brain regions related to olfaction (Leutgeb et al., 2015).

The current study has several limitations. First, because participants were selected based upon a threshold level of impulsivity, the results of correlations between that measure and other characteristics are unlikely to reflect, in terms of the strength of association, what might be found within a more unbiased and representative population. Second, as this study is cross-sectional, no conclusions can be drawn with respect to causation. Third, all TBI data derives from history provided by the participants which is subject to a range of errors and biases, although we have previously reported evidence to suggest that offenders’ reports of past TBI have reasonable validity (Schofield et al., 2011).

We did not examine for peripheral olfactory disorders or other neuropathological disorders that could impact olfactory performance and our health survey did not include the details of the covariates of olfactory ability, such as medication and history of sinonasal injury; surgery was not controlled for. However, the health survey included the smoking history of all the participants and 83% of them were tobacco users (73% former and 10% current). The olfactory testing in this study relies on the verbal ability to identify the specific odor and a full measure of olfactory ability such as olfactory discrimination and olfactory acuity test would give a better understanding of the relationship between the current study’s sample and olfactory ability. We lacked a control group (i.e., non-impulsive non-offenders) which limits our ability to draw conclusions about the specificity of our findings with respect to the male and impulsive offender population and we lacked any brain imaging. Finally, because the study participants were characterized by elevated levels of impulsivity, we considered the possibility that impulsivity itself might affect olfactory performance, i.e., by participants not paying due attention to the testing process itself, and thereby making careless errors that were behavioral rather than olfactory perceptual. We hoped that the influence of impulsivity on the process of olfactory testing would be negligible, given the limited number of items in the short SS test.

In terms of practical applications, as we have discussed elsewhere, moving from the findings from group studies of olfaction and its correlates to considering the potential benefits of OI testing of individuals raises many questions and challenges (Ramaswamy and Schofield, 2022). The clearest benefit of OI is to detect olfactory impairments that would confer risk from failure to detect hazards such as smoke or spoiled food. If it were to be established by history that hyposmia/anosmia immediately followed a TBI, this would imply the probability of a more severe brain injury, especially if it was not accompanied by facial injuries (that might be responsible for a peripheral olfactory nerve injury). Interpreting the result of OI, at the individual level would mandate a minimum set of questions, many of which were not asked in the current study, including whether (and if so in what context) the sense of smell was lost or diminished. The history that anosmia or hyposmia closely followed a viral respiratory infection (a common scenario) would be vital information relative to the possibility that the olfactory changes are a marker of important OFC brain dysfunction (i.e., post-viral anosmia does not predict brain damage). Some people are unaware of olfactory impairment, however, and a negative history (e.g., an individual reports no history of TBI or of post-viral olfactory loss) is much more valuable than having no history at all. In the context of the criminal justice system, where individuals who enter the system have often previously sustained TBIs, a low performance on OI if done, might add weight to reports of a past severe TBI, or imply a severity when not reported or unknown. Finally, if anosmia were identified in an entrant to the criminal justice system, without any explanatory history, it might raise a flag to prompt further considerations as to the possibility of some relevant brain pathology. Although a very rare scenario, the olfactory loss can be due to a frontal tumor that may also cause behavioral changes (Snyder et al., 2000). In the context of current criminal justice system practices, where screening for important neuropsychiatric conditions tends to be limited (especially for cognition), weighing the cost benefits of OI against other competing needs would be challenging in the absence of more data and studies.

In conclusion, our study showed that, relative to population norms, impulsive violent offenders as a group performed more poorly on a test of OI. Their performance on this test was associated with other exposures (TBI, childhood sexual abuse) and other behavioral measures in patterns that would be consistent with olfaction serving as a proxy for OFC functioning. The possible role of olfactory testing within studies of offenders, or in their routine screening, warrants further consideration. In future studies we plan to examine whether olfactory test scores can aid in the prediction of offending, and whether they might contribute to the prediction of response to sertraline, in terms of offending reduction, within the ReINVEST study.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving humans were approved by these independent Ethics Committees: UNSW Human Research Ethics Committee (HREC) (HC11390 and HC17771), Aboriginal Health and Medical Research Council HREC (822/11), and Corrective Services NSW HREC (09/26576). Approval from the NSW Justice Health and Forensic Mental Health Network HREC (G8/14) will allow participants to continue the study while in detention. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.

VC: Conceptualization, Formal analysis, Writing – original draft. TB: Conceptualization, Funding acquisition, Methodology, Supervision, Writing – review & editing. BT: Data curation, Project administration, Writing – review & editing. KW: Funding acquisition, Writing – review & editing. PM: Funding acquisition, Writing – review & editing. LK: Project administration, Writing – review & editing. DG: Funding acquisition, Writing – review & editing. AE: Funding acquisition, Writing – review & editing. VG: Funding acquisition, Writing – review & editing. PS: Conceptualization, Funding acquisition, Methodology, Supervision, Writing – review & editing.