[Insert Figure 3 here]
A few inconsistent MMN findings are worth mentioning. First, some people
‘recover’ without repeated psychotic episodes, and they do not exhibit
an abnormal MMN (Kim et al., 2020). This highlights a key gap - few
longitudinal studies have been conducted to ascertain how biomarkers
change over time or with vacillating symptoms. Second, a small study in
the subclinical population reported that high scorers on the
suspiciousness subscale had larger MMN amplitudes than low
scorers (Broyd et al., 2016). Thus, the current literature presents
competing perspectives: 1) that increased symptom load reliably predicts
abnormal MMN (e.g., (Claridge & Beech, 1995), but 2) in the subclinical
population more subtle patterns of preserved and impaired MMN emerge.
Clearly, more research is needed to address these gaps in our
understanding.
Oculomotor and Low-Level Visual
Deficits
Despite the wealth of data cataloging impaired auditory SM in
schizophrenia and SSD, there is relatively little in the visual SM
domain. This is surprising given the prevalence of oculomotor deficits
in schizophrenia, suggesting that the visual system is affected. Before
describing the studies that have reported on visual SM, we note research
pinpointing oculomotor deficits in SSD. We address this issue first
because oculomotor deficits lead to atypical sampling of the environment
and these contribute to abnormal visual sensation. Oculomotor responses
are disrupted along SSD with atypical performance in saccadic tasks
(e.g., double-step, adaptation, anti-saccade) and smooth pursuit
(O’Driscoll & Callahan, 2008; Thakkar & Rolfs, 2019; Wolf et al.,
2021). A proposed mechanism is that abnormal corollary discharge (e.g.,
(Feinberg, 1978) disrupts knowledge about eye position, resulting in
inaccurate eye movements with more interruptions during visual tracking.
Findings in nonhuman primates and lesion studies implicate impaired
signaling in the mediodorsal thalamus, which serves as an intermediary
between subcortical eye movement control areas (e.g., superior
colliculus) and frontal eye fields (Thakkar & Rolfs, 2019).
Inactivating this pathway creates a mismatch between where an organism
believes their eyes are directed and where they are actually looking and
thus alters visual perception (Cavanaugh et al., 2016). In those with
schizophrenia the abnormal visual scan patterns of faces and social
settings contribute to aberrant social interactions (Patel et al.,
2020). Oculomotor deficits contribute to higher order cognitive deficits
because those with schizophrenia sample and perceive the environment
abnormally.
Approximately ~60% of individuals with schizophrenia
have distortions in visual perception (Phillipson & Harris, 1985) and
>33% experience visual hallucinations (Silverstein & Lai,
2021). The range of perceptual deficits is broad and includes worse
performance in assessments of contrast sensitivity (Harper et al.,
2020), detection of contour (Keane et al., 2014), color (Fernandes et
al., 2019), biological motion (Okruszek & Pilecka, 2017) but see
(Keane, Peng, et al., 2018), faces (McCleery et al., 2015), and stronger
afterimages (Thakkar et al., 2021). The extent of afterimage deficits is
clinically relevant as they predict illness severity (Keane, Cruz, et
al., 2018).
Similarly, accounts for visual deficits in schizophrenia spectrum
disorders identify abnormalities in the anatomy of the retina (reviewed
in reviewed in (Bernardin et al., 2017; Silverstein et al., 2020), as
well as atypical network-level connectivity, both hypo- and hyper-
connectivity, including cortical - medial temporal lobe abnormalities
(reviewed in: (Silverstein & Lai, 2021). Together, the consistent
oculomotor and low-level visual deficits suggest that processing from as
early as the retina is abnormal in schizophrenia.
Visual Sensory Memory Biomarkers of Symptom
Severity
Given the range of oculomotor and low-level visual deficits identified
in SSD, it is surprising how little work has been conducted in iconic
memory. Several studies investigating iconic memory decay in those with
schizophrenia have reported no differences in schizophrenia (Hahn et
al., 2011; Knight et al., 1978). We know of no research evaluating
iconic SM in schizotypy in the general population .
Similarly, it is noteworthy that in comparison to the high volume of
research on the auditory MMN, there is little research assessing the
visual MMN in schizophrenia and in SSD. However, atypical visual MMN are
documented and confirm that abnormal responses are not isolated to the
auditory system. For example, the visual MMN is significantly reduced in
individuals with schizophrenia in an oddball task using letters as
stimuli (Neuhaus et al., 2013), visual motion direction (Urban et al.,
2008) or horizontal compared to vertical grating patterns as oddballs
(Farkas et al., 2015), with a similarly large effect size in group
differences. The same pattern of reduced MMN amplitude has been
characterized in studies using emotional faces (Csukly et al., 2013; She
et al., 2017; Yin et al., 2018), in which the MMN reduction correlates
with behavioral performance on an emotion recognition task (Csukly et
al., 2013). One recent finding reports that individuals with
schizophrenia showed normal visual MMN elicited by fearful faces but
diminished amplitude MMNs elicited by neutral faces (Vogel et al.,
2018). A new study has now identified larger visual MMN to happy
compared to sad and neutral faces and found that MMN amplitude to the
happy faces correlated with schizotypy scores, and interestingly, with
measures of autism characteristics, highlighting the difficulty with MMN
and specificity of diagnosis (Ford et al., 2022).
Another ERP that is linked to sensory memory is the P1. Visual P1
responses were significantly smaller in schizophrenia in response to low
(but not high) spatial frequency gratings that was not related to visual
acuity (Farkas et al., 2015). Although the P1 amplitudes did not
correlate with symptoms, they were related to cognitive performance, as
well as education level, duration of illness, and measures of global
functioning (Farkas et al., 2015). Visual MMN has also been elicited in
response to changes in the direction of moving dots and is significantly
reduced in schizophrenia (Urban et al., 2008). Visual MMN reduction was
again associated with global functioning, general symptoms, and
medication dosage (Urban et al., 2008), highlighting the parallels
between visual and auditory MMN. Despite these similarities across the
modalities, we found no findings describing the visual MMN in other SSD
or high schizotypy participants.
In summary, despite notable visual and oculomotor involvement in SSD,
and a wealth of data demonstrating auditory SM deficits, little
attention has been paid to visual SM specifically and no evidence
of atypical iconic memory in SSD. Expanding visual SM research in the
SSD population is needed to complement the auditory SM work and to
deepen our understanding of visual SM contributions to other aspects of
cognition.