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THE PERCEPTIONS MODULE OF PERCEPNET PROMOTES CRITICAL DISCUSSION ABOUT HOT ISSUES IN SENSORY SCIENCE AND PERCEPTION, THROUGH MONTHLY CONTRIBUTIONS OF OUTSTANDING RESEARCHERS AND PROFESSIONALS.
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A Sensational Crisis

Part I: The Evidence
[Una crisis de los sentidos]
Óscar Vilarroya

In a not very distant past, very few people would dispute what I will call the Perception Dogma, or the dogma for short. Say that we focus on visual perception. The idea was that a certain information would be registered at the retina, then the result of such a process would be sent on up to the primary visual cortex, and then up to associative areas until some sort of representation was formed in some part of the cortex.

Common to all variations on this view of perception, there was a clear distinction between some sort of “primary” stage, that was called sensation, and a cognitive one that was called perception. More concretely, the transduction of physical energy (e.g., light, sound, pressure, etc.) in the environment into neural signals and codes would correspond to sensation. This would have to be distinguished from the interpretation of those signals and codes, which is what would correspond to perception. Thus, while we would sense lights, sounds, tastes, smells and touches, we would perceive them as, say, a chocolate ice-cream or a glass of lightly chilled Burgundy.

It seems now without question that contemporary neuroscience is changing such a view, not only in relation with visual perception, but also in all sensory modalities. The research that is being conducted in developmental neurobiology, neurophysiology and cognitive neuropsychology is suggesting that the processes involved in perception are so intermingled that there is little value in trying to divide them up neatly into sensation and perception. Among other things, the research has shown that there is a strong processing of feed back processing of information between final and initial stages of the perceptual process, as well as between different sensory modalities.  In short, the evidence blurs the boundaries between sensations and perceptions.

The present paper is divided in two parts. In the first one I will present recent evidence that is changing completely the traditional way of characterizing perception. In the second part, to be published shortly, I will outline the elements for a new conceptualization of perception.

Unidirectionality of perception?

Neuroanatomists have always known that there are massive feedback pathways projecting from “higher”, associative, cortical areas to “lower”, primary, cortical areas. True, the anatomy and physiology of the details of connections among all the different perceptual areas are still subject of intense investigation. Nevertheless, it is a fact that anatomical research has shown that, for example, the ascending pathways from the retinal to the geniculate nucleus and from there to the visual cortices and to other centers higher in the processing hierarchy are matched by descending pathways from the higher level of processing to even the earliest processing systems at the retina (Zeki 1978; Van Essen 1985). Additionally, the mammalian visual system has been seen to consist of a large number of cortical areas which that are interconnected by many pathways, some of which can be characterized as bottom-up, and others as top-down (Felleman and Van Essen, 1991).  Moreover, the bottom-up projections constitute only a small minority of all synapses into cortical areas, whereas the top-down connections seem to be more abundant and diffuse (König and Luksch 1998; Douglas and Martin 1998).

However, these anatomical facts have been greatly ignored from the point of view of perceptual processing. At most, it has been proposed that such feed-back projections served only as a sort of modulating influence. This is so because, according to a dogma’s hypothesis  known as the impenetrability thesis of perception (Fodor 1983), perception is a bottom-up process and cannot receive top-down influences. The hypothesis asserts that higher cognitive processes, the systems of belief and knowledge, have little or no impact on processing in sensory-motor systems, because sensory systems are impenetrable.

Contrary to this conclusion, however, recent evidence indicates that higher cortical areas affect the content of sensory-motor systems directly. The primary cortex is not anymore a mere relay station when certain information is processed and re-directed to other parts of the cortex. There is a dynamic interplay between the brain’s so-called early sensory areas and the higher perceptual centers. In this sense, recent experiments in awake behaving animals (von Stein et al 1997) have shown that the coupling between different levels of visual perceptual areas depends on the expectancy of the individual. In particular, a feedback interaction in form of increased synchronization was found between primary visual areas and associative areas. The functional mechanism and the consequences of the interactions remain unclear, but it seems that primary visual areas can, and may need, be influenced by associative areas to function properly (Gilbert 1998).

In humans, studies (Zacks et al 2001) suggest that the perception of certain high-level stimulus need the simultaneous activity in primary regions (the extrastriate motion area MT or V5), and higher associative areas (the frontal eye fields, FEF). This research has tapped into a network of brain processes that involves top-down expectations and  bottom-up motion cues as a simultaneous processing. All these processes may contribute to the ability to form perceptual distinctions, and favor a top-down interpretation in which perception is determined by knowledge of the stimuli.

Additionally, neuroscience research on mental imagery has demonstrated that the primary visual cortex, V1, is often active, along with many other early visual areas (e.g., Kosslyn et al 1995). In motor imagery, the primary motor cortex, M1, is often active, along with many other early motor areas (e.g., Crammond 1997; Deschaumes-Molinaro et al 1992; Jeannerod 1994, 1995). Indeed, motor imagery not only activates early motor areas, it also stimulates spinal neurons, produces limb movements, and modulates both respiration and heart rate. For example, when proficient shooters imagine shooting a gun their entire body behaves similarly to actually doing so. In auditory imagery, activation has been observed in the primary auditory cortex (Calvert et al 1997) and activation has been observed in other early auditory areas (e.g., Zatorre et al 1996).

Memory also seems to play an active role in perception. Considerable evidence suggests that specific experience early in life can influence the perceptual processing of basic perceptual stimuli, such as orientation and tilt, in visual perception, or auditory illusions (Blakemore & Cooper1970; Sengpiel et al 1999;  Merzenich  et al. 1984; Gilbert and Wiesel 1992; Darian-Smith & Gilbert1994; Gilbert et al 1996; Whitaker and McGraw). Likewise, in perceptual anticipation, the cognitive system uses past experience to simulate a perceived entity's future activity. For example, if an object traveling along a trajectory disappears, perceivers anticipate where it would be if it were still on the trajectory, recognizing it faster at this point than at the point it disappeared, or at any other point in the display. Recent findings indicate that knowledge affects the simulation of these trajectories. When subjects believe that an ambiguous object is a rocket, they simulate a different trajectory compared to when they believe it is a steeple (Reed & Vinson 1996). Even infants produce perceptual anticipations in various occlusion tasks (Hespos & Rochat 1997).

Research studies by Karni and Sagi (1995), Yeo, Yonebayashi, and Allman (1995), Antonini, Strycker, and Chapman (1995), Stiles (1995), Merzenich and Jenkins (1995) also show that changes can be induced in visual cortical neural patterns in response to learning. In other words, visual processing at all levels may undergo long-term, experience-dependent changes. One type of learning is known as “slow learning”. This type of learning causes structural changes in the cortex, with  formation of new patterns of connectivity. Such a learning can result in significant performance improvement; for example, one may learn with practice to perform better at visual skills involving target and texture discrimination and target detection, and to learn to identify visual patterns in fragmented residues of whole patterns (priming). Performance in these tasks was thought to be determined by low-level, stimulus-dependent visual processing stages. The improvement in performance in these tasks, thus, suggests that practice may modify the adult visual system, even at the early levels of processing. As Karni and Sagi remark “[L]earning (acquisition) and memory (retention) of visual skills would occur at the earliest level within the visual processing stream where the minimally sufficient neuronal computing capability is available for representing stimulus parameters that are relevant input for the performance of a specific task” (1995, pp.95–6).

All of these results reinforce the idea that perception cannot be seen as a bottom-up process in which each stage is independent of the next. The results further indicate that top-down and bottom-up processes coordinate the processing of useful perceptions.

Domain-specificity of perception?

Many textbooks on perception consider each sensory modality -vision, hearing, etc.- in isolation, as if each modality processed its information without relevant interactions with other senses.  However, integration among different modalities is not only a common phenomenon in the brain, but it is also prerequisite for many types of perception and behavior.  Of course, nobody questions that at some level there is some sort of integration between different modalities (such as that the concept [rose] could include visual and olfactory cues). The dogma asserts that the sensory processing respects modality boundaries. This is sometimes referred to the modularity hypothesis (Fodor 1983).

The word "module" is a sort of battle field for many cognitive theorists. As it is recognized by nearly everybody, the term “module” is used in markedly different ways by different schools of thought and by different scientific disciplines. This fact has not helped the interdisciplinary discussions of cognition.  In neuroscientific terms, a "module" refers to some neuroanatomical characteristics in which brains are structured, with cells, columns, layers and/or regions that divide up the labor of information processing in a variety of ways. 

In cognitive science and linguistics, the term "module" refers to another view, which is normally attributed to Jerry Fodor's (1983).  A Fodorian module is a specialized, encapsulated mental sub-system that has evolved to handle specific information.  Fodor argues that perceptual sub-systems are one of such a structure, and lists a number of properties which are characteristic of a cognitive system's being modular, the most important of which are: (i) informational encapsulation (i.e., modules have little or no access to the background beliefs and goals of the larger organism), (ii) domain specificity, (iii) unconsciousness (modules provide very limited information about the processing steps) and (iv) innateness.  There are other criteria which does not interest us here, such as speed of processing (modules are very fast),  obligatory firing (modules operate reflexively, providing pre-determined outputs for pre-determined inputs regardless of the context),  ontogenetic universals (i.e. modules develop in a characteristic sequence), localization (i.e. modules are mediated by dedicated neural systems), and pathological universals (i.e. modules break down in a characteristic fashion following some insult to the system).

The claim in Fodor's version of modularity about information encapsulation and domain-specificity of perceptual sub-systems is contradicted by recent neurophysiological and neuropsychological evidence. There are many research results that show that the very sensory processing of each modality interacts normally with other modalities.

Crossmodal integration of multisensory cues (for instance, visual and auditory) is one of these examples. In the crossmodal integration two or more modalities are integrated in the same process. Many research results suggest that crossmodal integration is not only a fact, but it is also necessary in perceptual processing in early stages (Driver 1996; Vroomen and Gelder 2000; Macaluso et al 2000).

One of the most famous examples is the McGurk effect, where seen lip-movements can alter which phoneme is heard for a particular sound, while in the ventriloquism effect, they can alter the apparent location of speech sounds.

A recent study in humans (Calvert et al 1997) has also shown that perceiving a speaker’s lips during face-to-face conversation (lip-reading) activates auditory cortex in normal hearing individuals in the absence of auditory speech sounds.  Moreover, the experiments carried out by Calvert and colleagues suggest that these auditory cortical areas are not engaged when an individual is viewing nonlinguistic facial movements but appear to be activated by silent meaningless speechlike movements (pseudospeech). In other words, these experiments suggest that silent lip-reading activates auditory cortical sites also engaged during the perception of heard speech. This supports psycholinguistic evidence that seen speech influences the perception of heard speech at a prelexical stage.

The crossmodal effects are not restricted to the auditory modalities. Among others, there have been studies that found that the superior colliculi integrates cues from three sensory modalities, vision, audition and somatosensation (Wallace et al 1996; Sparks & Groh 1995), and others experiments show that visual perception can be qualitatively altered by sound (Shams et al 2000). The ventriloquist effect  can also be obtained by visual and  tactile cues (Radeau 1994; Spence, Driver  2000;  Pavani, Spence, Driver  2000). Likewise, the McGurk-like effects happens with for non-speech stimuli, as when both hearing and seeing musical instruments (Saldaña and Rosenblum 1993). Perturbing the sounds made as hands are rubbed together can affect the perception of skin texture, while changing the color of drinks or food can alter the perception of their flavor  (Jousmäki, Hari 1998; DuBose, Cardello, Maller 1980).

As for the chemical senses studies reveal perceptual processes responsive to combinations of odors and tastes (Gielen et al 1983; Stevens, 1997; Guadagni et al  1963; Murphy 1977). One of the best examples of such an integrative process may be flavor perception, whereby activation in two peripherally distinct neural systems, olfaction and gustation, combines to give rise to an unified perception. It has been argued that the integration may happen in a post-sensory stage, but recent studies show that crossmodal summation of subthreshold concentrations of selected gustatory and olfactory stimuli happen at the very early stages of the perceptual processing, thus demonstrating that integration of taste and smell occur all along the perceptual processing (Dalton et al 2000). Crossmodal integration seems to be the rule rather than the exception.

Finally, there are recent studies that are even more intriguing, since they suggest that all perceptual processes can be modulated and affected by emotional cues. In short, perceptions may be influenced by the emotional significance of an impinging stimulus. Adam Anderson and Elizabeth Phelps (2001) have shown that the amygdala supports emotional influences directly on  perception itself. Their research shows for the first time that perceptual systems are exquisitely tuned to the occurrence of emotionally significant stimulus events, requiring much less attention or effort to reach conscious awareness compared to events of neutral value.

Boundaries between perception and cognition?

But there is more. Not only top-down influences on perceptual processes are normal, but even (dogmatic) perceptual abilities can be performed by (dogmatic) sensory processes. A recent study (Freedman et al 2001) pose, for example, a major problem for current models of visual processing. In particular, it implies that a great deal of categorization processing can be done on the basis of the perceptual visual sub-systems. Freedman and colleagues examined the responses of neurons in the prefrontal cortex (PFC) of monkeys trained to categorize animal forms (generated by computer) as either "doglike" or "catlike." By continuously "morphing" the basic form of one animal into the other, the authors were able to identify  neurons that responded to category membership rather than simple processing of the physical characteristics of the images.

One of the most impressive features of their research is the speed at which the categorization responses took place.  Monkeys categorized stimuli very quickly, with reaction times that average 250 to 260 milliseconds but that can be as short as 180 milliseconds. The areas implicated were the lateral geniculate nucleus of the thalamus (LGN), V1, the so-called primary visual cortex, areas V2 and V4 of the ventral visual pathway,  areas in the posterior and anterior inferior temporal cortex (ITC) and the prefrontal cortex (PFC). This does not allow much time for complex iterative processing and suggests that the initial activation of cells in ITC and PFC could depend largely on a feed-forward pass through the visual system. This kind of data has strong implications for our understanding of visual processing because it implies that the visual pathway must be acting as a sort of pipeline processor, with different images being processed simultaneously at different levels of the system. 

Likewise, recent research shows that even the systems of belief, knowledge, attention and consciousness modulate perception. For example, conceptual representation of an ambiguous perceptual stimulus biases sensory processing. In audition, when subjects believe that multiple speakers are producing a series of speech sounds, they normalize the sounds associated with each speaker (Magnuson & Nusbaum, 1993). In contrast, when subjects believe that only one speaker is producing these same sounds, they do not normalize them, treating them instead as differences in the speaker's emphasis. Thus, each interpretation produces sensory processing that is appropriate for its particular conceptualization of the world. Again, cognition and sensation coordinate to produce meaningful perceptions.

Analogous interpretative effects occur in vision. Conceptual interpretations guide computations of figure and ground in early visual processing (Peterson & Gibson 1993); they affect the selective adaptation of spatial frequency detectors (Weisstein & Harris 1980); and they facilitate edge detection (Weisstein & Harris 1974). Frith and Dolan (1997) report that top-down interpretative processing activates sensory-motor regions in the brain.

Conclusion

In sum, we have seen a number of empirical studies that show three ways in which the dogmatic perceptual framework loses ground. First, we have seen that perception is influenced by a top-down flow of information, which intervenes in many different functional directions. Secondly, we have seen how crossmodal sensory integrations is not only a fact, but it may be even a requirement.  Finally, there may be some cases in which higher cognitive activities, such as categorization, are performed in the very same perceptual processing.  The conclusion could not be more clear: A new conceptualization of perceptual processes is called for.

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1/10/01
[SUGGEST-AN-ISSUE]
[Part II:
The Proposal]
 
 
 
 
 
 
 
 
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