The retrieval of learned information—A neurophysiological convergence-divergence theory

J. theor. Biol. (1976) 56, 95-110

The Retrieval of Learned Information--a Neurophysiologieal Convergence-Divergence Theory J. GRINBERG-ZYLBERBAUMt

Brain Research Laboratories, New York Medical College, 106th Street and Fifth Avenue, New York, N.Y. 10029, U.S.A. (Received 21 May 1974, and in revisedform 20 December 1974) The information in the brain is associated with specific patterns of electrical activity, resulting from the firing characteristics of neurons and circuits located in a tridimentional complex space. The external world is represented in this space after an energy transformation. From this representation, common features are extracted by way of convergent circuits. These circuits concentrate in few neuronal elements information that prior to their activation is distributed in a great deal of neurons. The convergence circuits are arranged in a hierarchical order in which each one of them receives information from the previous. In each hierarchical level of convergence, more abstract and concentrated characteristics of the information is handled. At some levels, the convergence circuits from various sensory modalities interact by way of polisensory neurons. Thus, language and complex associations are derived from them. The retrieval of stored information involves the activation of these high convergence polisensory circuits that in turn stimulate divergence circuits that duplicate similar patterns of neuronal activity as the ones activated when the now retrieved information was perceived.

1. Introduction Each object that is perceived is transformed in the retina in a complex but specific spacio-temporal pattern of neuronal activation. This complex pattern contains all the information a b o u t the object. The subjective perception takes place when the complex pattern o f neuronal activation arrives to the cerebral structures in which the analysis a n d decodification o f the pattern is done. The retrieval and evocation o f the stored information a b o u t the object arises when some parts or perhaps all the pattern activated, is duplicated by way o f some stimulus that triggers it. In this sense, the perceptual process is inseparable from the complex retrieval process. Experimental evidence in I" Present address: Prisciliano Rodrtguez 20 Tepoztlan Morelos, M6xico. 95

96

J. GRINBERG-ZYL]3ERBAUM

accord to this postulation was first obtained in a study made by Livanov & Poliakov (1945) in which the so-called "assimilation of the rhythm" phenomenon was described. Following a classical conditioning association procedure, a cortcial EEG rhythm of 3 c.p.s, began to appear when a conditioned stimulus was applied, and later on was observed even during the intertrial intervals. These facts seem to point towards the interpretation that the frequency of the electrical rhythm contained the information about the stimulus. Furthermore, Yoshii, Prover & Gastaut (1957) found that the assimilation of the rhythm phenomenon was aroused when an animal was placed in the site in which it was conditioned but it did not arise in a non associated place. This finding means that the electrical activity that represents information can be triggered and retrieved by parts of the stimuli complex present during the acquisition of the learning paradigm. The fact that the same rhythm appeared during the real presentation of the stimulus and in its absence, but in the presence of part of the stereotype that was associated with it, indicates that the brain acquires a representation of the stimulus complex, that corresponds with the particular electrical activity that is released during the retrieval. In more recent work, John's research group has presented evidence (Chow, Dement & John, 1957; John 1967, 1972; John, Bartlett, Shimokochi & Kleinman, 1973; John & Killam, 1959, 1960; John, Leiman & Sachs, 1961; John, Ruchkin & Villegas, 1964) that extends the latter findings. In one of their earliest approaches (John & Killam, 1959), they conditioned cats~to avoid an electrical shock by responding to a flickering light of 10 c.p.s. When this light attained a cue value, it was observed that the electrical activity of the visual cortex and other structures began to correspond to the frequency of the light. Later on when another frequency of the flickering light was introduced and the animal made a generalized response to it manifesting the same avoidance behavior, the electrical activity corresponded to the interprctation (informational content) that the animal gave to the stimulis and not to its physical characteristics. That is to say, the electrical activity was the same as the one recorded when the stimulus was actually of 10 c.p.s. When the animal began to differentiate the new light by not responding to it, the electrical activity began to correspond to the physical characteristics of the now differentiated stimulus. This means, that the actual informational value of one stimulus is related to its capacity to evoke stored information, and this in turn is well correlated with the patterns of electrical activity that are evoked by it. The informational value of the electrical rhythms seems to be independent of the particular learning paradigm used. This fact was demonstrated in a study by John & Killam (1960) in which animals were conditioned to press a lever in response to a stimulus of 10 c.p.s, and not

RETRIEVAL

OF I N F O R M A T I O N

IN THE BRAIN

97

press it when it was of 6 c.p.s. In the initial presentations of the 6 c.p.s. stimulus, when the animals responded to it as if it were of 10 c.p.s., the electrical activity of the cortex, lateral geniculate, reticular formation, hippocampus and fornix corresponded to the one recorded when the 10 c.p.s. stimulus was actually presented. This means that the real informational value of a stimulus complex is not associated with its physical characteristics, but instead with its capacity to release a previously stored representation, manifested in a particular and specific electrical rhythmical activity. The behavioral interpretation that one animal makes about a stimulus represents the particular form in which the stimulus is integrated and perceived. The correlation between the representation and the electrical activity that is associated with it indicate the important informational content of this activity. On the other hand, the studies above mentioned indicate that the perception processes are inseparable from the retrieval processes associated with stored information. Only this interdependence explains why the same physical stimulus results in different behavioral outcomes. The idea that the codified information about an external stimulus is related to particular patterns of electrical response is also supported by the studies of Colavita (1973) in which an external conditioned stimulus of specific frequency that has been utilized as a conditioned one, is substituted by direct electrical stimulation of the brain at the same frequency. This direct stimulation evoked exactly the same response as the one obtained with the external stimulus. Furthermore, if the behavioral paradigm implies responding in two different forms to two distinct external stimuli that differ in frequency, the direct stimulation with the two frequencies result in the two behavioral responses, each one controlled by the internal frequency in the same way and specificity as the two external ones. The pattern of electrical activity that is aroused when a stimulus acquires informational value does not depend upon the physical characteristics of the stimulus, but instead upon the way that it is interpreted. This "interpretation" in neurophysiological terms must involve some mechanism that transforms the incoming signal in the pattern of neuronal activity that corresponds to the stimulus complex with which it has been associated. The incoming signal establishes some interaction with a stored pattern. This latter pattern is the one that appears and not the one that corresponds to the physical characteristics of the external stimulus. Herrington & Schneidau (1968), studying humans, found that the visually evoked responses differed in wave shape depending if the stimulus that arouse them was a circle or a square equated in area. If the subject was later asked to imagine a square or a circle each time a flash illuminated a blank field, clear reproducible differences in wave form were produced to T.B.

7

98

J. G R I N B E R G - Z Y L B E R B A U M

each of the imagined figures and they resembled the waveforms obtained with the actual stimulus. This ingenious study indicates that the real perception and the imagined one (that is the retrieved one) are accompanied and related to the same type of electrical activity. If the electrical rhythmical activity and the waveform of the evoked potentials are so nicely correlated with the informational content of a stimulus, we can expect the unitary activity from which the latters result (Fox & O'Brien, 1965; Morrell, 1967) to manifest similar relations. Perhaps the most clear and thoughtful study in this respect is the well known research done by Morrell (1967). In the first stage of his study, Morrell recorded the activity of single cells in the visual cortex (visual area III) of the cat during the application of visual, acoustic and tactil stimuli. A great majority of the cells studied were polisensory in the sense that they responded to different modalities of stimulation but they manifested particular response patterns that were specific and different depending on the stimulus used. The response patterns differed even for stimuli of one modality but with different characteristics. Thus a vertical bar with a length of 3.6 cm moving from left to right in a dark room gave a different response pattern from the one obtained from the same stimulus but moving in the opposite direction. Once the above facts were determined and the specific response patterns of the cells responding to different stimuli were recorded, the author began to stimulate his animals with combinations of stimuli. The cells response to the combined stimuli had extremely complex patterns that in some cases resembled a simple linear summation of the firing patterns for each separate stimulus, although the majority of the cases were more complicated than the ones expected to arise from a simple sum. The combined or associated presentation of the stimuli were usually repeated until two blocks of 20 trials each were given. Following this procedure, the "preferred" stimulus of the pair was presented alone. In approximately 10~o of the cells studied, the single presentation of this stimulus evoked stable response patterns with a marked resemblance to those elaborated by the combined stimuli. If the presentation of the single stimulus was continued without being associated with the other member of the pair, the response pattern began to resemble the one obtained prior to the association maneuver. But if the combined presentation was now reinstalled, very few trials were necessary to achieve the transformation in the response pattern. These facts indicate that the firing pattern of a neuron can be changed by an association procedure. Furthermore, the changes obtained resemble the response aroused during the combined or associated presentation. Thus the patterns of neuronal activity represent the end product of stored experiences and are not the result of the unchangeable and direct physical characteristics of the stimulus.

RETRIEVAL

OF INFORMATION

IN THE BRAIN

99

A very interesting fact arising from this same study is that the cells that displayed the capacity of combining and storing the associated pattern were only those with a polimodaI character, that is the ones that responded previously to any manipulation to the stimuli that were later on associated. John (I972) discusses this fact as evidence that suggests that the crucial event in learning is not the establishment of new connections between cells but the enacting of a new pattern of activity in the already existing connections. This postulation is in accordance to the findings of Hubel & Wiesel (1963) and Wiesel & Hubel (1963, 1965) about the fact that in very young visually inexperienced kittens, the cells of the visual cortex respond in a normal fashion to complex visual stimuli, as if the neuronal circuits associated with these responses existed prior to birth, but if the cat does not use these circuits, they begin to deteriorate. 2. The Retrieval of Stored Information in the Nervous System There are different types of retrievals of stored information. One of them is the phenomenon associated with saving in relearning. A second type involves the simple recognition of one stimulus complex. A third type occurs when the name of an object is evoked when this object is visually perceived or on the contrary, when the verbal information about an object arises an image of it. Finally, there is a redintegrative type of retrieval in which a complete reconstruction of some past experience is achieved. All of them arise as a consequence of the presentation of a previously associated stimulus that now triggers the activation of a memory store. If the information in the nervous system is represented as specific neuronal patterns of activation, then the stimulus that trigger's the retrieval must be capable of arousing them. The specific type of retrieval probably depends upon the capacity of the trigger stimulus to duplicate the exact pattern in a more or less complete form. Two questions must be answered before we continue: firstly, how does the trigger stimulus become capable of causing the retrieval ?; that is, the pattern. Secondly, on what does the exact duplication of it depend? To answer the first question, we must make an analysis of the characteristics of some sensory system, hoping that this analysis will help in arriving at some conclusion that could answer the question. The second problem will be treated later on. There are at least four different types of cells in the visual cortex of the cat (Eysel & Grusser, 1971 ; Hubel & Wiesel, 1965). The first type is known as simple. They are found mostly in the visual area 17 primary visual cortex (Hubel & Wiesel, 1965). Their fields are concentric (as the ones found in contrast cells in the lateral geniculate body) or elongated (Hubel & Wiesel,

100

J. GRINBERG-ZYLBERBAUM

1962, 1965). The position of the stimulus in the retina is very critical for these neurons. The orientation of the stimulus that evokes an optimal response in these ceils is also critical (Hubel & Wiesel, 1962). In the same area 17 and in the adjacent 18 (secondary visual cortex) there are complex cells. These units respond in a similar way as the simple cells do, but their fields are longer in size and never concentric in form (Eysel & Grusser, 1971 ; Hubel & Wiesel, 1962, 1965). The response of these cells is independent of the part of the field stimulated. It is very probable that the complex cells receive convergent information from simple cells; at least, this is the best explanation of the similarity of response and the increase in the size of the receptive fields. The third type of cells are the low order hypercomplex units, found in areas 18 and 19 (tertiary visual cortex). They respond, as do complex cells, to a slit and edge or a dark bar, but the length of the stimulus is critical. The optimal stimulus is thus a critically oriented line falling within a given region of the retina. Similar stimulus in adjacent portion are inhibitory to it (Hubel & Wiesel, 1965). The responses of these cells are explained by assuming convergent circuits arising from complex cells, some being facilitatory and some inhibitory. The fourth type of cells are the high order hypercomplex units. Their responses resemble the ones found in lower order hypercomplex cells, but differ when responding to the line in either of two orientations, 90° apart (Hubel & Wiesel, 1965). They are found mostly in tertiary cortex and as the lower order cells; they respond optimally to directionally moving stimuli. The size of the receptive fields of the higher order ceils is much longer than the one found in lower order units and their response does not vary in respect to the part of the field stimulated (Eysel & Grusser, 1971). In general, the behavior of the higher order cells is as though they receive their input from a large number of lower order hypercomplex cells (Hubel & Wiesel, 1965). The independence of response in these cells in relation to the localization, of the stimulus in their receptive fields means that these neurons are not influenced by localization. This fact can be explained by the assumption that neurons that respond to a complex stimulus, converge in them. The organization of the cat's visual cortex is columnar. Each vertical column contains similar cells in relation to their complexity, best orientation of the stimuli, etc. (Hubel & Wiesel, 1962, 1965). Similar findings have been reported in the monkey (Hubel & Wiesel, 1968; Wurtz, 1969). The field size of the complex cells in these animals is larger than that of the simple units and smaller than that of the hypercomplex cells (Hubel & Wiesel, 1968). It is supposed (Hubel & Wiesel, 1968) that the simple cells receive convergent information from concentric cells in the lateral geniculate body. The complex ones receive convergent information from the simple cells. The

RETRIEVAL OF INFORMATION IN THE BRAIN

101

lower order hypercomplex cells receive convergent information from complex cells and the high order hypercomplex ceils receive convergent information from lower order hypercomplex cells (Hubel & Wiesel, 1968). These high convergence circuits explain the increase in complexity from simple to high order hypercomplex cells and the increase in receptive field size. In informational terms, this increase of convergence means that very complex information is concentrated in fewer channels as we move from the periphery to the central portions of the system. In this sense, relatively few cells contain the same information that was previously related to the activity of a much greater number of elements. This "concentration" of information is perhaps done at the expense of complicating the neuronal pattern of response in the high convergence units. The visual information does not remain and stop at the level of the tertiary visual cortex, there is evidence that indicates that the visual cortex projects itself onto other structures (Curnod, Casey & McLean, 1965; Chalupa, Harvey & Lindsley, 1972; Dow & Dubner, 1969; Gross, Rocha-Miranda & Bender, 1972; Hubel & Wiesel, 1969; Kass, Hall & Diamond, 1972; Pribram, 1972); this evidence also shows that the response of the cells in some of these structures can be more complicated (in terms of the optimal stimulus that makes them respond) than the ones recorded in area 19 (Gross et al., 1972). For example, it has been found in monkeys that some cells of the inferotemporal cortex respond in an optimal way to the presentation of a visual pattern that resembles a monkey's hand (Gross et al.,1972). This evidence indicates that perhaps the convergence circuits are maintained and exaggerated at this level. This means that the information is more concentrated in these structures and it contains the information associated with the activity of the previous ones. Other structures in which the concentration of information may take place are the pulvinar nucleus and the caudate nucleus (Buckwald, Rakic, Wyers, Hull & Heuser, 1962; Chalupa et aL, 1972; GrinbergZylberbaum, Carranza, Cepeda, Vale & Steinberg, 1974; Grinberg-Zylberbaum et al., 1973; Kaas et aL, 1972; Pribram, 1972). Similar processes seem to be associated with the auditory system. In this system, it was found (Evans, 1971) that in the peripheral structures, the cells respond to relatively simple sounds (i.e. pure tones), while the responses of the cells in the auditory cortex are associated to much more complex sounds. These are units that respond in optimal form to a sound that varies its frequency in a sequential form. The optimal sequential variation occurs in the sense of increasing, and/or decreasing, the pitch. These types of responses can only be explained if these ceils receive convergent information from cells that respond to each of the frequencies of the complex sound. Furthermore, the fact that they respond specifically to an increase or to a decrease in the sequence of

102

J. GRINBERG-ZYLBERBAUM

frequency, is explained by assuming the existence of lateral inhibitory circuits that become activated only when the activation of the cells is in some preferred sequence. Here again, as we move away from the peripheral portion of this system, there is an increase in convergence that makes the reduction in the number of channels that convey complex information possible. The auditory information (as the visual one) probably does not remain in the auditory cortex. There is evidence about the existence of extra auditorycortical areas that respond to sound stimuli (Albe-Fessard, Oswaldo-Cruz & Rocha-Miranda, 1960; Albe-Fessard, Rocha-Miranda & Oswaldo-Cruz, 1960; Bental & Bihari, 1963; Grinberg-Zylberbaum et al., 1973; Sedwick & Williams, 1967; Thompson, Johnson & Hoopes,1963; Thompson, Smith & Bliss, 1963). Perhaps some of them receive very complex and previously integrated auditory convergent information. If as stated before, both the visual and the auditory systems have as a characteristic the increase of convergence, and if the convergence circuits of the two systems establish a mutual communication at some level in the nervous system, then a functional interaction between them becomes possible. The communication is probably made with polimodal-polisensory units in which the association of patterns can be achieved. The existence of polisensory neurons and of common brain areas of interaction between the auditory and visual modalities is a well known fact in actual neurophysiology. Cerebral structures such as the pulvinar nucleus (Allman, Kaas, Lane & Miezin, 1972; Chalupa et al., 1972; Wright, 1971), inferotemporal cortex (Gross et al., 1972; Pribram, 1972), caudate nucleus (Albe-Fessard et aL, 1960a, b; Encabo & Buser, 1964; Grinberg-Zylberbaum et al., 1973; Schiller & Stryker, 1972), reticular formation (Hernandez-Peon, 1955, 1961; Yoshii et al., 1957), "association cortex" (Bental & Bihari, 1963; Thompson et al., 1963a, b) and even the visual cortex (MorretI, 1967; Murata, Cramer & Bach y Rita, 1965) fulfil the latter characteristics. Furthermore, if the polisensory neurons are of the same class and capabilities as those described by Morrell (1967) then not only an association between patterns becomes possible but also a triggered duplication of them. This postulation may be better understood in the following example. Imagine a man that has never seen a flower. The first time that we show him a rose, he certainly is able to see it although he does not know what it is and what it is called. The vision of the rose resulted from the complex and specific activity of the man's visual system, at least from the activity of the simple, complex and hypereomplex neurons in the cortex. At the same time that we present the rose, we give him verbal information... "This is a flower." If the verbal pattern "flower" is pronounced each time that our hypothetical man sees the rose, there will be a moment in which it will be enough to present the visual information (in the absense of

R E T R I E V A L OF I N F O R M A T I O N I N THE B R A I N

103

the verbal one) for the man to s a y . . . "this is a flower". By the same token, it will be enough to present the verbal information (in the absence of the visual one) for the man to imagine a rose. In this case, the image of the rose is the retrieved visual memory of the previously perceived flower and the verbal pattern is only the stimulus that triggers and arouses this memory. In the previous case, the verbalization ("This is a flower") is the retrieved verbal memory of the previously heard name, and the visual object is only the stimulus that triggers and arouses this memory. In order to have the visual or the verbal evocation of the flower, it is necessary to reproduce the same or similar neuronal patterns of activation that normally occur when we give the verbal or the visual information. In this particular case, the neurons of the primary, secondary and tertiary visual cortex, or the corresponding cells in the auditory one must become activated with similar electrophysiological patterns to the ones corresponding with a real perception. If this is true, then definitely the neuronal verbal flower pattern must be enough to give place to the visual rose and/or the neuronal visual rose pattern must be enough to give place to the verbal one. The real presentation of a flower activates millions of receptors at the retinal level. This activation converges into the axons of the optic nerve and after passing through the lateral geniculate body, arrives to the primary visual cortex where a great number of simple type cells begin to respond. The activation of these cells converge into the complex ones and their activity activates the convergent circuits that are connected with the hypercomplex neurons. From here the highly concentrated visual information travels to high convergence polisensory neurons that at the same time receive highly concentrated verbal patterns. The cells so activated respond with a complex pattern that is a sort of combination of both and because of this, contains them. By a process previously unknown, these cells can store the combined pattern and respond to each one of the single stimulus with it (Morrell, 1967). This does not mean that memory is contained in a private form in some neurons; I think that these units participate in a lot of evocation processes; the specific memory that is evoked is probably dependent upon the specific pattern of activation that arrives to them and triggers their response. The activation of the polisensory neurons and the display of the highly concentrated information contained in their pattern of response, is perhaps the first step in the process of retrieval and evocation of stored information. If the retrieval process stops at this level, surely neither visual image nor a verbal manifestation is obtained. For these to take place a more complete and duplicated activation of the patterns must take place. We now face a most delicate and difficult problem that was already

104

J. GRINBERG-ZYLBERBAUM

mentioned in a previous section: how is the exact duplication of the cerebral cortex patterns achieved? First of all, the previously postulated existence of high convergence polimodal cells in which the association between patterns takes place, has a logical and theoretical value. The association processes are much easier, exact and economical in a system of relatively few elements that contain very complex and concentrated information, than in one that contains a giant number of cells in which the information is dispersed and fractioned between the elements that constitute it. At the same time, the most logical way to explain how the duplication of the patterns in the cerebral cortex is achieved as a result of the polimodal cells responses, is by postulating the existence of divergence circuits from those neurons to the cells of the cerebral cortex. If this hypothesis is true, then the hypothetical divergence circuits to the cortex must be activated in a specific form when a particular combined pattern of activation arises in the high convergence polimodal cells. Perhaps the rhythm, frequency and other characteristics of the patterns in these neurons are able to "open" and make respond specific divergence circuits. This "opening" could be related to the specific refractory periods or the capacity to follow certain frequencies in the neurons conforming the divergence circuits, so a change in the codification of the polisensory neurons could be the critical factor that determines which divergence circuits become active and which characteristic patterns of responses arise in them. All the ideas mentioned could explain why, when someone tells us to have an image about a flower we can see a rose and why when we see a rose we can mention the word flower. Obviously, the word flower can stimulate the image of a lot of different flowers or parts of them so that the image is very rarely complete and clear. This means that the accurate and total reproduction of the visual stored pattern is very difficult to achieve, being the activation of only some parts of the patterns the most common, probably those parts that are common to all the flowers. The accurate and total reproduction of the visual or other modality stored patterns and the specific type of retrieval (see the section about types of retrievals) achieved, probably depends on the fulfilment, more or less, of at least the following conditions: (1) the exact duplication of the pattern in the polisensory neurons; (2) the same state of excitability of the divergence polimodal-cortex circuits during the acquisition and during the retrieval of perceptual information; (3) the complexity of the stored information. The last point is understandable because it is easier to evoke the word flower when we see a rose than to imagine a rose when we hear the verbal-

RETRIEVAL

OF I N F O R M A T I O N

IN THE BRAIN

105

ization; perhaps this fact is related to the different quantity of divergence circuits that must be activated in the visual or the auditory systems. The necessary duplication of the state of excitability in order to have the reproduction of the patterns and so the retrieval of information is very well illustrated in the so-called state dependent learning experiments, where an animal executes a learned response only if he is submitted during the evocation session to the same conditions that occurred during the acquisition one (i.e. drugged state). On the other hand, there must be some logic in the activation of the patterns; this logic is perhaps related to the number of stimuli associated or combined. I think that the memory of one event is this logic of activation and it is not located either in the cerebral cortex or the polimodal structures but has to do rather with the specific patterns in all the systems. In this sense, the polimodal neurons are prepared to respond with a combination of patterns when one member of the association is presented; this would be the readout of memory. The combined pattern in turn and by way of divergence circuits, activates the structures that normally are involved in the "perception" of stimuli: these would be the evocation processes, and all together constitute the memory of one event. One process that is difficult to explain in this hypothetical model, is the characteristics of the divergence circuits. One possibility is that the divergence circuits are in some way the same but inverted as the convergence ones. This means that the activation can be initiated in the polisensory cells. From here the high order hypercomplex neurons are activated; later the low order hypercomplex ones, and finally the complex and the simple cells are also activated. If the portions of the cerebral cortex so activated are related to its columnar organization (Hubel & Wiesel, 1965) and each column is associated to a particular feature of the stimulus, then the quantity and the specific spacio-temporal organization of the columnar activation gives the appearance of a particular evoked image. Each column in its activation represents the "perceptual units" from which a complex image is constructed. The specific activation of a mosaic of columns may be the basic and fundamental process of perceptual and retrieved reconstruction of the external world. Depending upon the state of excitability of the divergence circuits, one or another image would be retrieved and so different memories would be evoked. Only if the state of the system remains the same as the one existing in the original activation during the perception phenomenon then the information that is evoked is the same. Another possibility is that the activation of the cerebral cortex as a result of the activity of the polimodal cells is by means of some intermediary structure. In the visual system this structure could be either the superior colliculus, the pulvinar, the inferotemporal cortex or the lateral geniculate body and from here using the normal pathways, the visual cortex.

106

J. GRINBERG-ZYLBERBAUM

The recent finding of John et al. (1973) about the clear and replicable appearance of the readout potential in the lateral geniculate body is perhaps a manifestation of the above processes; The emphasis placed in the cerebral cortex as the structure that needs to be activated in order to have a complete retrieval of stored visual information is based on the experiment of Herrington & Schneidan (1968) (see the evoked potentials section in this paper). Here, a duplication of the morphology of a scalp recorded evoked potentials (most probably arising from the cerebral cortex) was found when a geometrical figure was actually presented or an imagined retrieved one was suggested, and also the fact that the lesion in the visual cortex produces a blind condition in humans. Obviously, this evidence is not enough to validate the above idea. Research on the capacity to retrieve visual information in human beings who have been recently lesioned in the visual cortex is one way in which this hypothesis can be proved. On the other hand, the idea that polimodal cells contain and participate in the codification of visual information, and that their activity is necessary in order to activate the retrieval of stored information is now under experimental study in several laboratories. In a recent experiment (Grinberg-Zylberbaum et al., 1974) the electrical activity of the caudate nucleus of rats was disorganized by applying single square electrical pulses, while these animals were watching other rats pressing a lever in a Skinner box. The stimulation of this polisensory structure impaired this learning by observation. This study indicates the important participation of this structure in the integration of visual information. The retrieval of stored information is never a static enterprise, when we remember the image of an object as a result of a verbal order, we do not see a stable photograph of it, but instead a sequence of internal dynamic visions that have movement. This movement and dynamics seems to be independent but triggered by the verbal pattern. The independency is in the sense that the verbalization, in the majority of cases, does not have the explicit sequence in spite of the obvious fact that the image does. In the same way, when we remember the name of an object while we see it, the verbalization is a sequence of specific sounds in a particular order. If as stated before the activity of the polimodal cells is the beginning of the retrieval process, this activity must change and contain the appropriate sequence. The neuronal processes responsible for the retrieved sequence are unknown but perhaps they arise as a result of a memory sequenciator that stores them in separate depots that interact and trigger the activity of the high convergence polimodal cells. Perhaps this hypothetical sequenciator is related to eye movements. In this respect and concerning the visual recognition processes, Noton & Stark (1971) have postulated the following hypothesis: "The internal representation or

R E T R I E V A L OF I N F O R M A T I O N IN THE B R A I N

107

memory of an object is a piece meal affair: it is an assemblage of features or, more strictly, of memory traces of features. During recognition (we could add: retrieval) the internal representation is matched serially with the object, feature by feature. The features of an object are the parts of it (such as the angles and curves of line drawings) that field the most information. The memory traces that record the features are assembled into the complete internal representation by being connected with other memory traces that record the shifts of attention required to pass from feature to feature, either with eye movements or with internal shifts of attention; the attention shifts connect the features in an order of preference forming a feature r i n g . . . " It can be proposed that the presentation of verbal information that triggers a visual retrieval, simultaneously activates the high convergence polimodal cells and the sequenciator memory store whose activity determines the sequence of combined patterns of response in the polisensorial neurons. One cerebral structure whose activity is probably related to the above processes is the superior colliculus, because of its relationship with the eye movement regulation (Wurtz & Goldberg, 1972a,b) with the attention phenomenon (Goldberg & Wurtz, 1972) and its anatomical connections with the retina and the cerebral cortex (Michael, 1972). Finally, the existence of convergence circuits points toward a hierarchical organization of the brain in which each stage of convergence extracts common features of information. This extraction is plausible if we think that a neuron that receives signals from other neurons, responds with enhanced probability when a coincidence (spatial and temporal) of discharges arrives to it. In this sense, each level of the hierarchy handles more "abstract" information by concentrating in a single pattern of response the information that in previous levels is more "dispersed. It is possible to conclude that at some level of the convergence hierarchy, language and concept formation develops. Recently the first evidence of meaning extraction in the brain were experimentally obtained (Johnston & Chesney, 1974; Grinberg-Zylberbaum & John, 1974). In these experiments, it was found that the frontal, and temporal parietal human cortices extract language and conceptual meaning from the occipital representation of the visual world.

3. Related Phenomena (A) DUPLICATION OF INFORMATIOH IN THE VISUAL SYSTEM

The visual system has an enormous capacity for functional recovery after a partial lesion. This recovery is perhaps related to the duplication of information associated with the divergence circuits that exist from the

108

J. GRINBERG-ZYLBERBAUM

geniculate body to the occipital cortex (Chow, Blum & Blum, 1950). In the same way, the finding that a 98 ~o lesion of the optic nerve does not impair complex visual discrimination behavior in cats (Norton, Frommer & Galambos, 1966), means that the channels that carry visual information have their duplicity as a distinctive characteristic. This fact is in accord with the idea that the basic mechanism or process that represents information in the nervous system is not the activation of specific units but the appearance of a neuronal pattern of activation. (13) VISUAL AND AUDITORY RETRIEVAL OF INFORMATION DURING PARADOXICAL SLEEP

The appearance of visual images and auditory information during paradoxical sleep is one of the most remarkable characteristics of this stage of the sleep-wakefulness cycle. This appearance is perhaps related to the activation of stored electrical patterns in the auditory and visual cortices.The facility of these patterns to appear during this stage is perhaps a result of an increase of excitability in the divergence circuits related to the retrieval of information. This increase in excitability can be the same one that causes an increase in the magnitude of the thalamo-cortical potentials (Jouvet, 1967) and in the frequency of the spontaneous unitary activity during the same sleep stage (Jacobs, McGinty & Harper, 1973). Furthermore, artificial increments in the number of paradoxical stage periods have been observed as a result of the lesion of the caudate nucleus in rats (Corsi, Grinberg-Zylberbaum & Arditti, 1975). This fact is in accordance with the above interpretation, because of the evidence that shows that this structure has a normal inhibitory influence on the excitability of thalamo-cortical circuits (Demetrescu, Demetrescu & Iosif, 1965; Demetrescu, 1967; Heuser, Buchwald & Wyers, 1961). Perhaps the same or similar increments in excitability as a result of decrements in inhibitory network activity explain the appearance of visual and auditory illusions and even hallucinations in some "pathological" conditions as schizophrenia. (C) CONTROL OF COMPLEX MOVEMENTS

Certain complex patterns of movement are entirely programmed at the level of the spinal cord (Burke, 1973, personal communication). The corticalsubcortical system related to motor activity seems to send "orders" by way of the efferent system, that activate the spinal cord circuits related to them. Probably these "orders" are complex patterns of activation that are recognized by high convergence neurons that in turn activate specific motoneurons by means of divergence circuits. If this is true, then the motor activity can

RETRIEVAL OF INFORMATION IN THE BRAIN

109

be interpreted as a result o f a specific process o f retrieval of stored information. This situation is very similar to the postulation where the specific response of high convergence polimodal neurons with a complex pattern of activation, by means of divergence circuits, activate units in the visual or auditory cortices and so an image or a complex sound is retrieved. In fact, there is no logical reason to doubt that the activity of the nervous system is related to similar processes in all o f the structures and networks of which it is composed. The apparent dissimilar outcomes of its action are only related to the different characteristics of the effector organs but not to the nervous processes from which the activity of the latter results. This work was supported by the Mexican Science and Technology Council, CONACYT. REFERENCES ALBE-FESSAPa~,D., OSWALDO-CRuz,E. & ROCHA-MmANDA,C. (1960a). Electroenceph. clin. Neurophysiol. 12, 405. ALBEoFKSSARD,D., ROCHAoMIRANDA,C. d~ OSWALDO-CRuz, E. (1960b). Electroenceph. clin. NeurophysioL 12, 649. ALLMAN,J. M., KAAS,J. H., LANE,R. H. & MIEZ~, F. M. (1972). Brain Res. 40, 291. BENTAL,E. & BmARt,B. (1963). J. NeurophysioL 26, 207. BUCrlWAI.D,N. A., RAKIC,L., WYERS,E. J., HULL,C. & HEUSER,G. (1962). Expl Nearol. 5, 1. CrlALUPA,L. M., ANCrtELHARVEY& LINDSLEY,B. (1972). Expl NeuroL 36, 449. CHOW,K. L., DEMENT,W. C. & JOHN,E. R. (1957). J. NeurophysioL 20, 482. CHow, K. L., BLUM,J. S. & BLUM,R. A. (1950). J. comp. NeuroL 92, 227. COLAVXTA,F. B. (1973). Bull. psychon. Soc. 2, 109. CORSl, M., G~NnERG-ZYLnERnAUM,J. & ARDITrl, L. S. (1975). Physiol. Behav, 14, 7. CUENOD,M., CASEY,K. L. & MCLEAN,P. D. (1965). J. Neurophyshiol. 28, I101. DEMETRESCU,M., DEMETR~CU,M.. & IOSlF, G. (1965). Electroenceph. clin. Neurophysiol. 18, 1. DEMI~TrtEsCU,M. (1967). Brain Res. 6, 36. Dow, B. M. & DUBr,mR,R. (1969). J. NeurophysioL 32, 773. ENCABO,H. & BUSER,P. (1964). Electroenceph. clin. Neurophysiol. 17, 144. EVANS, E. F. (1971). In Pattern Recognition in Biological and Technical Systems, pp. 328-343. New York: Springer-Verlag. EYSEL,U. TH. & GRUSSER,O. J. (1971). In Pattern Recognition in Biological and Technical Systems, pp. 60-80. New York: Springer-Verlag. Fox, S. S. & O'BRIEN,J. H. (1965). Science, N.Y. 147, 888. GOLDBERG, M. E. & WURTZ, R. H. (1972). J. NeurophysioL 35, 542. GRINBERG-ZYLBERBAUM,J., CARRANZA,M. B., CEPEDA,G'. V., VALE,T. C. & STEINBERG, N. N. (1974). Physiol. Behav. 12, 913. GRINBERG-ZYLnERBAUM,J., PRAoo-ALCALA,R. & BRUST-C~MONA,H. (1973). Physiol. Behav. 10, 1005. GrUNBERG-ZVLBERBAUM,J. & JOHN, E. R. (1974). Unpublished data. GROSS, C. G., ROCHA-MIRANDA,C. E. & BENDER,D. B. (1972). J. NeurophysioL 35, 96. HERNANDEZ-PEON,R. (1955). Acta neuroL latinoam. 1, 256. HERNANDEz-PEoN,R. (I961). In Sensor), Communication, pp. 497-520. The Milit. Press and John Wiley & Sons, Inc. HERRINGTON,R. N. & SCHNEn3AU,P. (1968). Experientia 24, 1136.

110

J. G R I N B E R G - Z Y L B E R B A U M

HEUSm% G., BUCHWAt.D,N. A. & WYm~s, E. J. (1961). Electroenceph. clin. Neurophysiol. 13, 519. HUaEL, D. H. & WlF.SEL,T. N. (1962). J. Physiol. 160, 106. HUBEL, D. H. & WmSEL,T. N. (1963). J. of Neurophysiol. 26, 994. HtreEL, D. H. & WI~EL, T. N. (1965). J. of Neurophysiol. 28, 229. HUBEL, D. H. & WI~EL, T. N. (1968). J. PhysioL, Lond. 195, 215. HUBEL, D. H. & WI~EL, T. N. (1969). J. Physiol., Lond. 202, 251. JACOnS, B. L., McGn~rg, D. J. & HAR~ER, R. M. (1973). In Brain Unit Activity during Behavior, pp. 165-178. Springfield, Ill.: Charles C. Thomas. JOHN, E. R. (1967). In The Neurosciences--A Study Program, pp. 690-704. New York: The Rockefeller University Press. JoI-~, E. R. (1972). Science, N.Y. 177, 850. JOHN, E. R., BARTL~rr, F., SaIMOKOCm, M. & KLEINMAN,D. (1973). J. NeurophysioL 36, 893. Jom~, E. R. & I(dr.J_AM,K. F. (1959). J. Pharmac. exp. Ther. 125, 252. Jom~, E. R. & Kmt.~l, K. F. (1960). J'. nerv. ment. Dis. 136, 183. JOHN, E. R., LEn~tAN,ALL. & SACHS,E. (1961). Ann. N.Y. Acad. ScL 92, 1160. JOHN, E. R., RUCrIK~, D. S. & VmLEGAS,J. (1964). Ann. N.Y. Acad. Sci. 112, 362. JOHNSTON, U. S. & CHESNEY,G. L. (1974). Science, N. Y. 186, 944. JoowT, M. (1967). Physiol. Rev. 47, 117. KAAS,J. H., HALL, W. C. & DIAMOND,L. T. (1972). J. eomp. Neurol. 145, 273. LrVANOV, M. N. & POtaAKOV,K. L. (1945). Izv. Akad. Naak. SSSR Set. Biol. 3, 286. MICHAEL, C. R. (1972). J'. Neurophysiol. 35, 815. MORRELL, F. (1967). In The Neurosciences--A Study Program, pp. 452-470. New York: The Rockefeller University Press. MURATA, K., CRAMER,H. & BACH Y RrrA, P. (1965). J. Neurophysiol. 28, 1223. NORTON, T., FROMMER,G. & GALAMaOS,R. (1966). Fedn Proc. fedn Am. Socs exp. Biol. 25, 2168. 5, 263. NOTON, D. & STARK,L. (1971). Scient. Am. 224, 34. PRmRAM, K. H. (1972). Clin. Neurosurg. 19, 397. SCmLLER, P. H. & S3"RYKER,M. (1972). J. Neurophysiol. 35, 915. SEDWaCK,E. M. & WmLtAMS,T. D. (1967). J. Physiol., Lond. 189, 281. THOMPSON, R. F., JOHNSON,R. H. & HOOPES,J. J. (1963a). J. Neurophysiol. 26, 343. THOMPSON, R. F., SMrrH, H. E. & BLISS,D. (1963b). J. Neurophysiol. 26, 365. WI~EL, T. N. & Htra~L, D. H. (1963). J. NeurophysioL 26, 1003. WI~EL, T. N. & HUBEL, D. H. (1965). J. Neurophysiol. 28, 1060. WtmTZ, R. H. (1969). J. Neurophysiol. 32, 727. WURTZ, R. H. & GOLDBERt3, M. E. (1972a). J. Neurophysiol. 35, 575. WURTZ, R. H. & GOLDnERG, M. E. (1972b). J. Neurophysiol. 35, 587. YosHn, N., PROVOT, P. & GASTAUT,H. (1957). Electroenceph. clin. Neurophysiol. 9, 595.