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© 2010 Federation of European Psychophysiology Societies

G. G. Celesia:
Journal Visual Perception
of Psychophysiology 2010; and 24(2):62–67
Hogrefe
Vol. Awareness
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Article

Visual Perception and Awareness


A Modular System
Gastone G. Celesia
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

Chicago Council on Science and Technology, Loyola University of Chicago, IL, USA
This document is copyrighted by the American Psychological Association or one of its allied publishers.

Abstract. The study of visual processing and abnormalities due to lesions of cortical structures sheds light on visual awareness/con-
sciousness and may help us to better understand consciousness. We report on clinical observations and psychophysical testing of achro-
matopsia/prosopagnosia, visual agnosia, and blindsight. Achromatopsia and prosopagnosia reveal that visual cortices have functionally
specialized processing systems for color, face perception, and their awareness, and that furthermore these systems operate independently.
Dysfunction is limited to some aspects of visual perception; someone with achromatopsia, although not conscious of color, is aware of
the objects’ form, motion, and their relationship with sound and other sensory percepts. Perceptual awareness is modular, with neuronal
correlates represented by multiple separate specialized structures or modules. Visual agnosia shows that awareness of a complete visual
percept is absent, though the subject is aware of single visual features such as edges, motion, etc., an indication that visual agnosia is a
disruption of the binding process that unifies all information into a whole percept. Blindsight is characterized by the subject’s ability to
localize a visual target while denying actually seeing the target. Blindsight is mediated by residual islands of the visual cortex, which
suggests that sensory modules responsible for awareness can function only when structurally intact. We conclude (1) that perceptual
awareness (consciousness?) is modular, and (2) that perceptual integration is also modular, which suggests that integration among distinct
cortical regions is a parallel process with multiple communication pathways. Any hypothesis about consciousness must include these
observations about the presence of multiple parallel, but spatially and temporally different, mechanisms.

Keywords: consciousness, awareness, visual agnosia, cerebral achromatopsia, modular processing, blindsight, prosopagnosia

Introduction falsehood.” With these admonitions in mind, I emphasize


the existing knowledge based on clinical observations.
The definition of consciousness is a difficult and controver-
sial task. Most neuroscientists still agree with Huxley, who
in 1866 wrote: “What consciousness is, we know not”; and
with Crick and Koch (1990), who said consciousness is Methods
“the most mysterious aspect of the mind-body problem.”
Avanzini (1999) suggests that “we can define conscious- I limit my observations to the visual system, specifically to
ness as the awareness of self and of internal and external human data on conscious and unconscious visual percep-
environments organized in space and time categories.” In tion. The data reported here stem from my personal clinical
1994, Nobel Prize winner Francis Crick stated: “Now is the case studies gathered over the last 40 years. Institutional
time to think scientifically about consciousness (and its re- approval for experiment on humans was always obtained,
lationship, if any, to the hypothetical immortal soul) and, and each subject gave informed consent. The Helsinki dec-
most important of all, the time to start the experimental laration on human experimentation was adhered to in the
study of consciousness in a serious and deliberate way.” It gathering of data. Patients underwent a full neuro-ophthal-
is now possible to study “the nature and function of our mological examination, including visual acuity, and visual
subjective experience” (Güzeldere, Flanagan, & Gray field testing with V4e and I4e targets using Goldmann dy-
Hardcastle, 2000) that we call consciousness. namic perimetry. They were asked to draw a clock and a
I limit this report to conscious and unconscious visual daisy on an 8½ × 11-inch sheet of paper. Color testing was
perception as a method of promoting the understanding of evaluated with psychophysical techniques including Ishi-
consciousness, thereby trying to sort out reliable informa- hara pseudoisochromatic plates and L’Anthony’s desatu-
tion from pure speculation. Eccles (1970) suggested that rated panel D-15. Facial recognition was tested with five
any hypothesis must conform to “all existing knowledge”; US presidents’ portraits (Washington, Lincoln, Kennedy,
similarly Popper (1962) stated: “Coherence cannot estab- Nixon, and Reagan) and photographic pictures of family
lish truth, but incoherence and inconsistency do establish members; we also tested each patient with the picture com-

Journal of Psychophysiology 2010; Vol. 24(2):62–67 Hogrefe Publishing


DOI: 10.1027/0269-8803/a000014
G. G. Celesia: Visual Perception and Awareness 63

pletion from the WAIS. Visual evoked potentials (VEPs) to


alternating checks of 15 and 31 minutes of arc were record-
ed in most of the patients. Patient with blindsight had sac-
cade monitoring during the presentation of targets to the
blind and to the spared field. For details of the experimental
procedures we refer to prior publications (Celesia & Bri-
gell, 2005; Celesia, Bushnell, Toleikis, & Brigell, 1991).
Every patient underwent multiple MRI and CT as appro-
priate to determine the extent of cerebral lesions.

Results
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This document is copyrighted by the American Psychological Association or one of its allied publishers.

The data presented here can be subdivided into three topics:


(1) specific disorders of visual perception such as cerebral
achromatopsia; (2) deficit of visual integration such as vis-
ual agnosia; (3) blindsight.

Specific Disorders of Visual Gnosis Limited


to One Specific Aspect of Perception
These disorders (Celesia, 2005, 2007) include cerebral ach-
romatopsia, prosopagnosia, topographic agnosia, visual
language disturbances, and pure alexia. For brevity I limit
my presentation here to cerebral achromatopsia and pro-
sopagnosia. Cerebral achromatopsia is the failure to recog-
nize colors due to a lesion of the central nervous system.
The subjects are aware of their deficit and complain that
they see everything in black and white or in shades of gray.
Prosopagnosia is “a failure to recognize people known to
the patient on the basis of visual perception of their faces”
(Hecaen & Angelergues,1962). We report three cases of ce-
rebral achromatopsia (CA) due to cerebral ischemic in-
farcts. The subjects were tested repeatedly over 1 to 5 years
after the initial stroke. All patients had at least a superior
altitudinal visual field defect (Table 1), prosopagnosia, and
alexia without agraphia. The patients complained that they
could not see colors, but saw all images only in shades of
gray. As shown in Table 1, they all failed L’Anthony and
Ishihara’s color plates testing. They were able to imagine
objects in color, and two of them even claimed dreaming in
color. None of the subjects had any deficit in somatosensory
perception, audition, comprehension, or memory. MRIs of
the brain revealed a bilateral lesion involving the lingual,
fusiform gyri and part of the parahippocampal gyri (see
Figure 1).

Deficit of Visual Integration


The subject is a female aged 26 who developed severe head-
aches and had difficulty seeing. According to her mother, her
blindness had started on February 20, 2003. The patient could
not see her family members although she could see changes

Hogrefe Publishing Journal of Psychophysiology 2010; Vol. 24(2):62–67


64 G. G. Celesia: Visual Perception and Awareness
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

Figure 3. MRI of the lesions observed in the subject with


This document is copyrighted by the American Psychological Association or one of its allied publishers.

Figure 1. Diagram of the lesions observed in the three pa- visual agnosia (same subject as in Figure 2). Note the spar-
tients with cerebral achromatopsia and prosopagnosia. The ing of the striate cortices.
lesions were bilateral and involved both the lingual and fu-
siform gyri.
in the lighting. The patient stated that her sight appeared to be
black with occasional movements and lights. On February 22
she behaved as if blind, claiming she could not see, but when
pressed she was able to cooperate and agreed she has some
vision (Table 2). She stated that she could identify family
members and friends by their voice, but she could not “see”
them. When asked to draw from memory a daisy she drew a
circle and stated “that is not quite it,” though she did not know
why. When asked to copy drawing of shapes (circle, triangle,
square, etc.) she was able to do so, but could not identify any
of the shapes (see Figure 2) When asked to match images such
as a house and a cross, she did it correctly but then did not
know what the objects were. When looking at an illustration
she could not describe it and stated “I cannot make sense of
it.” She could not identify any of the Ishihara color plates. She
showed correct registration of the constituents of form, line,
and edge elements as well as their correct position and orien-
tation. She could at times identify a line drawing, but only in
isolation, not as a part of a whole illustration. She could not
Figure 2. 26-year-old woman with visual agnosia, who
“bind together” these form elements into a whole perception.
could copy alphabetic letters, numbers, and line drawings,
She had in fact visual agnosia, though she had no difficulties
but was unable to identify what she was seeing or drawing.
recognizing and interpreting perceptions from other sensory
Her drawing of a daisy was poor, and she realized “that is
systems (olfactory, auditory, and somatosensory). As shown
not quite it.” Her performance suggests that she could cor-
in Figure 3 she had bilateral lesions of the white matter in-
rect register form perception, lines, and edges as well as
volving most of the connections from and to the visual cor-
their correct position and orientation, but could not “bind”
tices. Areas 17, 18, 19, the lingual, fusiform, and parahippo-
together this information to identify the whole visual per-
campal gyri were intact.
cept.

Table 3. Visual performance in blindsight


Patient Age Localization Perception Pupillary Pupillary Recogni- PVEPs to PVEPs to PVEPs to VEP Map- Activation
with visual target of changes response response tion of any 15’ checks 31’ checks 60’ checks ping & am- of area 17 on
blindsight (forced in illumi- to light to Accom- visual per- plitude dis- PET/SPECT
choice) nation modation cepts tribution
Case KC 65 yes yes yes yes Absent Absent Absent Delayed nt yes
Case JB 81 yes yes yes yes Absent Absent Normal nt nt yes
Case GA 59 yes yes yes yes Absent nt Delayed nt Normal yes
Case TR 58 yes yes yes yes Absent Delayed Normal Normal Normal yes
Note: nt = not tested.

Journal of Psychophysiology 2010; Vol. 24(2):62–67 Hogrefe Publishing


G. G. Celesia: Visual Perception and Awareness 65

Figure 4. Regional cerebral blood


flow (rCBF) determined via positron
emission tomography (PET) in a pa-
tient with blindsight. rCBF is ex-
pressed in ml/100 g/minute. Four re-
gions of interest were selected,
roughly corresponding to the location
of areas 17, 18, and 19. The number
above each bar indicates the rCBF val-
ue. Note the increased rCBF with vis-
ual stimulation indicating neuronal ac-
tivation of the visual areas.
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This document is copyrighted by the American Psychological Association or one of its allied publishers.

Blindsight brain-damaged individuals provides results that cannot be


obtained in any other way. The three cases of achromatop-
Fendrich, Wessinger, and Gazzaniga (1992) define blind- sia and prosopagnosia show not only that the visual cortex
sight as the “residual visual capacity in the absence of ac- has functionally specialized processing systems for color
knowledged awareness.” We studied four subjects with and face perception and awareness, but also that these sys-
cortical blindness related to bilateral occipital infarcts. tems can “act fairly autonomously” (Zeki & Bartels,
They were able to localize visual targets although denied 1999a). Dysfunction of these systems does not affect au-
having seen them. They were not aware of what “their eyes ditory, olfactory, somatosensory, and other visual aware-
have taken in nor what their brain have processed” (Weis- ness not related to color or facial recognition. The subject
krantz, 1993). As shown in Figure 4, positron emission with achromatopsia, although not conscious of color, is
tomography (PET) showed increased cerebral blood flow aware of the objects’ form, motion, and their relationship
(rCBF) to visual stimulation with flashes and patterns in with sound and other sensory percepts. This indicates that
the primary visual cortex of one subject. Similarly activa- perceptual awareness is modular, with neuronal correlates
tion of the visual cortical areas was demonstrated by sin- of awareness represented by multiple specialized but sep-
gle photon emission computed tomography (SPECT) in arate structures or modules. Furthermore, these cortical
the other three patients. VEPs to pattern stimulation were processing areas are also perceptual sites. Zeki (2008)
recorded in all four cases. These patients (Table 3) had suggests that each of these systems represent its own “mi-
preserved visually evoked potentials to pattern and flash croconsciousness.” In two of our subjects mnemonic rep-
stimulation and had preserved rCBF in areas 17, 18, and resentations of prior experiences associated with color and
19. We concluded that visual information reached residual faces (imagining, dreaming) were preserved, suggesting
islands of primary visual cortex but did not reach aware- that these representations were stored in different regions
ness. than the fusiform and lingual gyri, and were thus accessi-
ble to the subject via separate pathways. The multifaceted
complexity of the visual perception is clearly shown by
the patients’ restricted visual deficit while preserving oth-
Discussion er visual consciousness/awareness. If visual awareness is
modular with specialized structures or modules for color,
As aptly stated by Crick (1994), there are many “forms of object, motion, and other features distributed both in space
consciousness, such as those associated with seeing, and time, to see a complete conscious visual percept there
thinking, emotion, pain and so on. Self-consciousness . . . must be a process that unifies or binds all this “microcon-
is probably a special case of consciousness.” The data pre- sciousness” into a complete visual consciousness. Should
sented here are confined to visual consciousness and based this hypothesis be correct, it follows that a disruption of
on clinical and psychophysical observation of brain-dam- this binding process interferes with the awareness of a
aged individuals. As stated eloquently by Zeki and Bartels complete visual percept, while preserving the awareness
(1999b): “Despite an increasing sophistication in the in- of single visual features such as edges, motion, etc. This
struments that are able to detect and measure cortical ac- is essentially what happened to our subject with visual ag-
tivity, a high and honorable place must still be reserved nosia: She showed correct registration of the constituents
for a much simpler and older technique, that of clinical of form perception – line and edge elements at their cor-
observation.” Psychophysical techniques such as visual rect position and orientation. She could at times even iden-
field perimetry, assessment of color vision, motion percep- tify lines in a drawing, but only in isolation, not as a part
tion, and other visuo-perceptual testing are indispensable of a whole illustration. But she failed to bind these form
to properly evaluating the visual system. The study of elements together into a whole percept. Feature extraction

Hogrefe Publishing Journal of Psychophysiology 2010; Vol. 24(2):62–67


66 G. G. Celesia: Visual Perception and Awareness

was preserved, but she was unable to integrate the various tual awareness of music is modular and separate from
aspects of the object into a complete image. The patient other auditory sensory perceptions.
had no difficulty integrating percepts from other sensory Auditory agnosia is less well defined, but it usually
systems (olfactory, auditory, and somatosensory). Rather, refers to impaired ability to recognize sound while having
her binding deficit was localized to the visual system. The a normal hearing. Clarke, Bellmann, Meuli, Assal, and
MRI showed that the visual cortices were intact, the bilat- Steck (2000) described a subject deficient in recognizing
eral lesions being localized in the white matter disrupting environmental sounds but with normal auditory localiza-
the input/output connections among the various visual tion and auditory motion perception. Ulrich (1977) de-
modules. The function of the network necessary for bind- scribed a case of auditory agnosia characterized by im-
ing was impaired. pairment of acoustic discrimination and amusia. Vignolo
Our four cases of blindsight are remarkable because (2003) reported that right hemisphere lesions tended ei-
they show that visual information reached the primary ther to disrupt the apperception of environmental sounds,
visual cortex as demonstrated by the presence of VEPs sparing music entirely, or to disrupt environmental
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sounds and melody, sparing rhythm, whereas left hemi-


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and the increased rCBF in the striate and extrastriate ar-


eas during visual stimulation with flashes or patterns. Yet sphere lesions tended to spare melody and to disrupt
the subject denied seeing any visual stimulus, although rhythm, either selectively or in association with the se-
able to localize the target. In our cases, blindsight was mantic identification of environmental sounds. Ulrich
mediated by residual islands of visual cortex; yet the cor- (1977) suggests that there is an analogy between auditory
tical modules were sufficiently damaged to prevent con- agnosia and the syndrome of “perceptive visual agnosia.”
scious perception. These cases suggest that the sensory These cases confirm that sensory awareness (microcon-
modules responsible for microconsciousness can func- sciousness) is processed by different modules, working
tion only when structurally intact. Additionally, the dis- separately but in parallel.
sociation between cerebral activation and perception cau- How the various modules are bound together remains
tions us about interpreting images of cerebral activation to be discovered. Neuroscience has shown that the pro-
as indicative of conscious perception. cess of sensory integration is a complex one that involves
But are these phenomena limited to the visual system? many other cortical areas with continuous feedback and
We need to address the issue of whether modularity is feedforward. Communication among different areas may
be conducted by gamma frequency oscillations. Synchro-
restricted to the visual system or is a general phenome-
nization at gamma and beta frequencies has been ob-
non. If the observations reported above exist in another
served in monkeys across several brain structures (Gre-
sensory system, we could assume that modularity is a uni-
goriou, Gotts, Zhou, & Desimone, 2009). Enhanced os-
versal event. Clinical observations in the auditory system
cillatory coupling (or synchronization) observed between
provide the answer: Amusia and auditory agnosia are dys-
prefrontal and visual cortex during attention had a shift
functions reported in the auditory system comparable to
in time of 8 to 13 ms allowing for spikes “initiated in one
the type of visual deficits just described. Amusia is the
area to affect cells at a peak depolarization phase in the
loss of musical talent (Hou, 2003) usually related to dam-
coupled area” (Gregoriou et al., 2009). Interactions be-
age to the temporal lobe. McFarland and Fortin (1982)
tween widespread neural regions in the brain is very fast
describe an accomplished organist who suddenly lost his
and “underlie fluid, organized behavior” (Knight, 2007).
ability to play familiar melodies as the result of an infarc-
tion of the right superior temporal and supramarginal
gyri. Schuppert, Munte, Wieringa, and Altenmuller In conclusion, neuroscience has shown from both clinical
(2000) investigated perceptual musical functions in pa- and laboratory studies in humans and primates that
tients suffering from unilateral cerebrovascular cortical 1. perceptual consciousness/awareness is modular,
lesions and found deficits in melodic and temporal musi- 2. perceptual integration (binding) is modular,
cal appreciation in left temporal lobe-damaged patients 3. integration among distinct cortical regions is a fast, fluid
and overall impairment of music perception in right tem- multipath process with communication pathways tuned
poral lobe-damaged patients. They concluded that recep- to different frequencies.
tive amusia indicate “autonomous, yet partially integrated
neural subsystems underlying the processing of melodic As Peissig and Tarr (2007) stated: “Despite this pro-
and temporal stimuli.” DiPietro, Laganaro, Leemann, and gress, the field is still faced with the challenge of devel-
Schnider (2004) reported amusia after a left temporal-pa- oping a comprehensive theory that integrates this ever-
rietal stroke in a professional musician. They described increasing body of results and explains how we perceive,
“preserved metric judgment and normal performance in recognize” and be conscious of objects, their surround-
all aspects of melodic processing,” while “he lost the ing, and our relationship to them. Any hypothesis con-
ability to discriminate or reproduce rhythms.” They con- cerning consciousness must include this knowledge
cluded that the temporal lobe does the “modality-specific about multiple parallel but spatially and temporally dif-
encoding of musical temporal information.” Thus percep- ferent mechanisms.

Journal of Psychophysiology 2010; Vol. 24(2):62–67 Hogrefe Publishing


G. G. Celesia: Visual Perception and Awareness 67

Encyclopedia of the neurological sciences (p. 122). Amster-


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