Download Why is Hubel and Wiesel`s description of the classical receptive field

Why is Hubel and Wiesel's description
of the classical receptive field inadequate
for an understanding of visual perception?
The Undergraduate Awards Submission
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Abstract
Receptive field is an area of the visual field that, when illuminated, alters the discharge rate
of a visual neuron. According to Hubel and Wiesel (1979), receptive field is a hierarchy
of cells in the visual cortex, cells divided into two major classes: simple and complex cells.
Simple cells are cells for which the optimal stimuli are lines of specific orientation rather than
the circular spots of light. More numerous than simple cells are complex cells, for which
the optimal stimuli are lines of specific orientation moving in a particular direction.
The implicit assumption of this structural description is that visual perception can be reduced
to activity of single, increasingly complex neurons. The essay aims at examining why Hubel
and Wiesel's description of the receptive field is inadequate. To fulfil that goal, Hubel
and Wiesel's work is compared and contrasted with later findings on visual neurons
and the organisation of the visual cortex. The essay concludes that, despite some correlational
evidence for Hubel and Wiesel's concept (Logothetis, Pauls, and Poggio, 1995),
their description of the classical receptive field is indeed inadequate. One-to-one mapping
between a complex visual stimulus and a neuron is statistically unlikely. Single neurons
can be affected by context and attention which is accounted for by the description
of the classical receptive field at all. At the higher level of the visual cortex organisation,
cortical streams (cortical areas, not single neurons) were shown to influence behaviours
of neuropsychological patients. Overall, this evidence demonstrates that Hubel and Wiesel's
description of the classical receptive field is inadequate because it is oversimplified.
Keywords: receptive field, visual perception, Hubel and Wiesel, cortex, grandmother cells
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Why is Hubel and Wiesel's description of the classical receptive field inadequate
for an understanding of visual perception?
Receptive field is an area of the visual field that, when illuminated, alters the discharge rate
of a visual neuron (Dowling, 2001). Hubel and Wiesel (1979) proposed a description
of the classical receptive field as a hierarchy of cells in the visual cortex. They divided them
into two major classes: simple and complex cells. Simple cells are cells for which the optimal
stimuli are lines of specific orientation rather than the circular spots of light. They are mostly
located in the V1 area of the cerebral cortex. More numerous than simple cells are complex
cells, for which the optimal stimuli are lines of specific orientation moving in a particular
direction. Complex cells are present in V1, V2, and other visual cortical areas (Dowling,
2001). Hubel and Wiesel (1979) suggested that the visual cortex operated locally and it was
not known how the entire brain synthesised the visual information. This view illustrates
the implicit assumption of their description of the classical receptive field: that visual
perception can be reduced to activity of single neurons. These single neurons are “feature
detectors” that respond to increasingly complex, specific stimuli. The essay aims
at examining why Hubel and Wiesel's description of the receptive field is inadequate.
To fulfil that goal, the essay compares Hubel and Wiesel's work with later findings on visual
neurons and the organisation of the visual cortex. The essay concludes that Hubel
and Wiesel's work is indeed inadequate. The reason is that their description of the classical
receptive field does not account for most of the subsequent more detailed evidence
on how the visual parts of the brain operate and what influences them.
The implicit assumption of Hubel and Wiesel's (1979) model, that visual perception
can be reduced to the activity of single neurons, is to an extent confirmed by later research
that, nonetheless, has to be interpreted with caution. Logothetis, Pauls, and Poggio (1995)
examined single neurons within the inferior temporal (IT) cortex, the brain region that plays
a role in the visual object recognition. They trained monkeys on a view of the 3-D object.
Then the subjects observed the rotated versions of the object. Measures of IT cells were taken
as the monkeys observed the object. When the preferred view was presented, the cells
discharged maximally, and their response decreased gradually as the object had been rotated
away from the preferred view. Logothetis et al. found a correlation between the neural firing
rate and recognition performance. Hence, they showed a link between unique cells and visual
perception consistent with Hubel and Wiesel's assumption of how the classical receptive field
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operates. However, Logothetis et al.'s results were correlational. They did not clarify
the causal nature of the relationship between cellular activity and perception. Additionally,
considering the finding of no selective cell response for consistently unrecognised objects,
it could be argued that Logothetis et al. did not show that individual IT cells are feature
detectors for a specific stimulus, i.e. a single 3-D object. Their results did not exclude
a possibility that activated individual cells belong to a distributed network of cells responding
to different aspects of the same stimulus. Altogether, this final interpretation is not consistent
with Hubel and Wiesel's description of the classical receptive field as consisting of single
“feature detectors.”
A further implication of Hubel and Wiesel's implicit assumption is that single complex
neurons (“grandmother cells”) address single complex concepts, e.g. a specific person (Gross,
2002; Quiroga, Kreiman, Koch, & Fried, 2008). Quiroga et al. (2008) argued
that the existence of “grandmother cells” is implausible for a number of reasons. First,
a Bayesian probabilistic argument (Waydo, Kraskov, Quiroga, Fried, & Koch, 2006) helped
estimate that the probability of finding a single cell discharging after a presentation
of a specific visual stimulus is extremely unlikely. Furthermore, a possible interpretation
of the pattern of cell firing is that they respond to classes of similar stimuli (e.g. faces
or landmarks), not to a single stimulus (consistently with the aforementioned interpretation
of a correlation found by Logothetis et al., 1995). A study of neurons in the medial temporal
lobe (MTL; Olshausen & Field, 1996) suggested that learning about stimuli developed
cellular units responsive to those stimuli. Quiroga et al. (2008) argued that, even though these
findings link neurons to unique stimuli, it is possible that the cells are not responsible
for recognition of a stimulus but for its memory storage. Quiroga et al. noted the latency
of the response in MTL after the onset of a stimulus in comparison to a rapid response in IT
(Hung, Kreiman, Poggio, & DiCarlo, 2005; Quiroga, Reddy, Kreiman, Koch, & Fried, 2005;
Thorpe & Fabre-Thorpe, 2001). They suggested that the delay results from high-level
processing that transforms visual information into memories in MTL. Altogether, Quiroga
et al. (2008) argued that the assumption of “grandmother cells” is implausible statistically.
Additionally, they offered a new interpretation of neural coding in MTL: it is sparse
but a single discharging neural cell and recognition of a specific complex stimulus cannot
be mapped one-to-one in the “grandmother cell” fashion implied by Hubel and Wiesel.
In case of neurons in MTL, the cellular activity may be related to different cognitive
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capacities than the one suggested by Hubel and Wiesel: it may be related to learning
and memory rather than to visual perception.
A further critique of Hubel and Wiesel's description of the classical receptive field
emphasises the role of attention in visual perception. Hubel and Wiesel did not address
it which makes their concept of the receptive field less accurate and hence less adequate
for an understanding of visual perception. However, studies have shown that attention affects
the response of individual neurons despite no change in the stimulation of the neurons'
receptive fields. Moran and Desimone (1985) demonstrated that effect by measuring changes
of the firing rates of neurons in the visual area V4. Monkeys kept their eyes fixed on the dot,
but paid attention to either the neuron's preferred or non-preferred stimulus. Their neurons
fired more intensively when monkeys paid attention to the preferred stimulus than when
it paid attention to a non-preferred stimulus.
Additionally, later research has shown a further shortcoming of the classical receptive field
concept. Kapadia, Ito, Gilbert, and Westheimer (1995) demonstrated that the change of firing
rates of visual neurons is related to context, another feature that, similarly to the influence
of attention on visual perception, was not considered by Hubel and Wiesel. Kapadia et al.
(1995) showed that the firing rate of a neuron of the monkey visual area V1 changed
in relation to whether the bar in the receptive field of a neuron was presented by itself,
surrounded by additional randomly distributed bars, or surrounded by bars that created
groups. The highest firing rate was detected in the first and the last condition where the bar
in the receptive field was not surrounded by random noise. These findings suggest that
the neuronal activity is sensitive to the influence of the context. Altogether, presented studies
show that context and attention affect visual perception, the results that Hubel and Wiesel's
description of the classical receptive field did not account for.
Having addressed problems with the description of the classical receptive field at the neural
level, the discussion can focus on the evidence against Hubel and Wiesel's concept from
the level of the visual cortex. Ungerleider and Mishkin (1982) proposed that cortical
pathways that conduct information from the primary visual cortex to the secondary
and association cortex belong to two streams: the dorsal stream and the ventral stream.
According to their “where” versus “what” theory of vision, the dorsal stream
(from the primary visual cortex to the posterior parietal cortex) is involved in the visual
spatial perception. The ventral stream (from the primary visual cortex to the inferotemporal
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cortex) is involved in the visual pattern perception. The theory was supported by evidence
from neuropsychological patients. Consistently with predictions made by the theory, patients
with damage to their posterior parietal cortex had difficulty reaching for objects that they
described with no difficulty, while patients with damage to their inferotemporal cortex
showed the opposite pattern of impairment (Ungerleider & Haxby, 1994). This evidence
implies that Hubel and Wiesel's description of the classical receptive field is inadequate
because complex streams and interconnections between cortical areas rather than unique
cellular structures guide visual perception. The elaboration and reformulation of Ungerleider
and Mishkin's (1982) theory that further highlights the inadequacy of Hubel and Wiesel's
concepts was proposed by Goodale and Milner (1992). They argued that the dorsal stream
was to control interaction with visual objects and the ventral stream was to specialise
in the conscious perception of objects. Goodale and Milner's theory gives two general
predictions. First, that damage to the dorsal stream disrupts behaviours towards visually
perceived objects and leaves the conscious visual perception intact. Second, that damage
to the ventral stream disrupts the conscious visual perception but not behaviours towards
objects. The support for the theory comes from neuropsychological cases. The pattern
of impairment in patient AT (Jeannerod, Arbib, Rizzolatti, & Sakarta, 1995) confirmed
the first prediction made by Goodale and Milner's (1992) theory. AT suffered from damage
to her occipitoparietal region which impaired her dorsal stream. Her conscious visual
perception was intact: she was able to demonstrate correctly the size of objects shown
to her with her fingers. However, her behaviour towards objects was impaired;
she was unable to grasp them because she oriented her hand movements incorrectly
in relation to the size of the objects. The pattern of impairment in patient DF (Goodale
& Milner, 2004) confirmed the second prediction made by Goodale and Milner’s (1992)
theory. DF suffered from damage to her ventral prestriate cortex which impaired her ventral
stream. She was unable to describe objects that she was to pick which suggests that she did
not perceive them consciously. However, she oriented her hand movements correctly towards
the objects that she was about to pick. This behaviour shows that her control of the visuallyguided behaviour remained intact. Altogether, discussed theoretical and empirical evidence
suggests that visual perception should be considered an interaction between cortical areas
and the use of visual information rather than, as Hubel and Wiesel (1979) suggested,
an interaction between neurons and types of visual information that neurons fire to.
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In conclusion, the essay has shown that, even though there is some empirical support
for Hubel and Wiesel's (1979) description of the classical receptive field, it is inadequate
for an understanding of visual perception. The general reason could be summarised
with Goldstein's (2002) view: Hubel and Wiesel's description is somehow crude; it assumes
a straightforward one-to-one mapping between a complex visual stimulus and a neuron.
However, such a case seems unlikely statistically. Moreover, context and attention
were demonstrated experimentally to affect single neurons, the results that Hubel and Wiesel
did not account for and did not predict. Importantly, the research that succeeded their work
moved from the correlation between levels of individual cell firing and recognition towards
neural networks and their engagement in learning and memory rather than visual perception.
At an even higher level, the organisation of the visual cortex into streams influencing visual
perception was demonstrated in more behaviourally-oriented studies. Neuropsychological
patients demonstrated the capacities of their visual perception with their behaviours guided
by vision, such as an ability to pick or describe an object. Altogether, diverse research
has demonstrated that Hubel and Wiesel's description of the classical receptive field
is not adequate for understanding of visual perception because it is oversimplified,
does not account for the roles of attention and context in visual perception, and overlooks
important complex interactions between cortical areas and the use of visual information
in cognition.
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