Neurodevelopmental Antecedents and Sensory Phenomena in Obsessive Compulsive Disorder: A Systematic Review Supporting a Phenomenological-Developmental Model

Abstract

<b><i>Background:</i></b> The majority of models on obsessive compulsive disorder (OCD) endorse a top-down perspective on the cognitive mechanisms underlying OCD functioning and maintenance, whereas a bottom-up perspective is rarely pursued. <b><i>Objectives:</i></b> The aim of the study was to review the empirical literature on sensory phenomena (SP) and neurodevelopmental antecedents of OCD, which could support the conceptualization of an alternative, bottom-up perspective integrating neurodevelopmental and phenomenological levels of analysis on OCD. <b><i>Methods:</i></b> A systematic review according to PRISMA guidelines was performed in PubMed/MEDLINE, PsycInfo, the Cochrane Library, and Excerpta Medica Database (EMBASE) and focused on SP and “neurodevelopmental antecedents” (operationalized in early risk factors, neuroimaging signs, neurological soft signs, and sensory responsivity). The time interval was from inception up to March 31, 2022. <b><i>Results:</i></b> From the search in electronic databases, 48 studies were retained and reviewed. SP are highly prevalent in OCD patients and overrepresented in comparison with healthy controls. Similarly, OCD patients also present a higher prevalence of early environmental adversities and sensorimotor alterations in terms of neurological soft signs and sensory over-responsivity in the tactile and acoustic domains; additional findings included hypogyrification signs at neuroimaging. Both sensorimotor alterations and SP are associated with tic-related manifestations and poorer insight in OCD patients. <b><i>Conclusions:</i></b> On the ground of established common subjective experience of SP and premorbid neurodevelopmental features, we hypothesized an explanatory model for OCD, which considers the possible pathophysiological role for altered corollary discharge and enhanced error detection in the neurodevelopment of SP and obsessions. SP may represent the subjective experiential resonance of an individual history of persistently inaccurate sensory predictions, whereas accompanying manifestations, such as the obsessive need for order and symmetry, may represent a compensatory attempt to mitigate SP. This neurodevelopmental-phenomenological bottom-up model, describing a dimensional gradient of sensorimotor alterations and related subjective experiences, may contribute to explain the dimensional affinity between OCD and schizophrenia spectrum disorders. Furthermore, this model could be useful for the early detection of subjects at higher risk of OCD.

Sensory Overresponsivity and Symptoms Across the Obsessive-Compulsive Spectrum: Web-Based Longitudinal Observational Study

“…Similarly, studies using magnetoencephalography in youth and adults suggest that individuals with OCD have altered sensory processing of auditory information compared with healthy individuals [51,52]. Although there is still little research on this issue, it can be stated that tactile and acoustic modalities of stimulation are the most investigated according to a recent systematic review focused on sensory phenomena in OCD [53].…”

SAPAP3, SPRED2, and obsessive-compulsive disorder: the search for fundamental phenotypes

“…Most contemporary models of OCD place a high degree of emphasis on the role of higher-level processes, such as cognitive flexibility or the sense of responsibility, in the genesis and maintenance of OCD symptoms. Such models can be considered as taking a “top-down” perspective (Poletti et al, 2022a ). However, OCD-like phenomena have been documented in animals, such as dogs, cats and primates (Luescher et al, 1991 ; Overall and Dunham, 2002 ; Lutz, 2014 ).…”

“…More generally, it is now understood that many of the symptoms of OCD may represent exaggerations or distortions of phylogenetically ancient adaptive behaviors or defense mechanisms, whose purpose is to ensure individual or group wellbeing and safety (Boyer and Lienard, 2006 ; Feygin et al, 2006 ; Stein et al, 2016b ). Such an evolutionary perspective regarding OCD entails a neurodevelopmental perspective, in which alterations in normal brain development could perturb basic, evolutionarily conserved neural processing systems and predispose to the development of OCD at specific stages of the life cycle in a “bottom-up” manner (Leckman and Bloch, 2008 ; Poletti et al, 2022a ). Such mechanisms could potentially be identified in animals as well as humans.…”

“…The consistency of these findings across rodents and humans suggests that at least some of the genetic mechanisms underlying OCD could be evolutionarily conserved. The fundamental phenotype involved in this process may represent lower-order deficits arising from alterations in neural development, which could influence higher-order cognitive processes in a “bottom-up” manner (Benzina et al, 2021 ; Poletti et al, 2022a , b ). These findings are also consistent with research suggesting that deficits in lower-order sensory and affective processing may underline the cognitive and behavioral changes seen in patients with OCD (Cavedini et al, 2012 ; Martoni et al, 2015 ).…”

Debate: The prevention of psychosis in child and adolescent mental health services

“…This expressivity, usually consistent with categorical diagnoses within the section of neurodevelopmental disorders (see DSM‐5), leads to CAMHS attendance for therapeutic interventions. For example, motor coordination disorders (Burton et al., 2016), attention‐deficit/hyperactivity disorder (Nourredine et al., 2021) and autism spectrum disorders (Foss‐Feig et al., 2019) are associated with a higher risk of psychosis in later years, as well as psychotic, affective and obsessive compulsive symptoms in adolescence, indicating a risk for later severe mental illness in adulthood, are usually preceded by premorbid neurodevelopmental antecedents in childhood (Parellada, Gomez‐Vallejo, Burdeus, & Arango, 2017; Poletti, Gebhardt, Pelizza, Preti, & Raballo, 2023).…”