Memory in astrocytes: a hypothesis
© Caudle; licensee BioMed Central Ltd. 2006
Received: 16 December 2005
Accepted: 18 January 2006
Published: 18 January 2006
Recent work has indicated an increasingly complex role for astrocytes in the central nervous system. Astrocytes are now known to exchange information with neurons at synaptic junctions and to alter the information processing capabilities of the neurons. As an extension of this trend a hypothesis was proposed that astrocytes function to store information. To explore this idea the ion channels in biological membranes were compared to models known as cellular automata. These comparisons were made to test the hypothesis that ion channels in the membranes of astrocytes form a dynamic information storage device.
Two dimensional cellular automata were found to behave similarly to ion channels in a membrane when they function at the boundary between order and chaos. The length of time information is stored in this class of cellular automata is exponentially related to the number of units. Therefore the length of time biological ion channels store information was plotted versus the estimated number of ion channels in the tissue. This analysis indicates that there is an exponential relationship between memory and the number of ion channels. Extrapolation of this relationship to the estimated number of ion channels in the astrocytes of a human brain indicates that memory can be stored in this system for an entire life span. Interestingly, this information is not affixed to any physical structure, but is stored as an organization of the activity of the ion channels. Further analysis of two dimensional cellular automata also demonstrates that these systems have both associative and temporal memory capabilities.
It is concluded that astrocytes may serve as a dynamic information sink for neurons. The memory in the astrocytes is stored by organizing the activity of ion channels and is not associated with a physical location such as a synapse. In order for this form of memory to be of significant duration it is necessary that the ion channels in the astrocyte syncytium be electrically in contact with each other. This function may be served by astrocyte gap junctions and suggests that agents that selectively block these gap junctions should disrupt memory.
Until recently astrocytes were considered to play no more than a supportive role for neurons in the central nervous system. This view has now been supplanted by a more active participation of astrocytes in information processing, where the astrocytes not only receive and respond to neuronal input, but also transmit signals to neurons [1–9]. These findings indicate that astrocytes contribute to the processing of information. In support of this concept it was recently demonstrated that spinal cord astrocytes are necessary to support hyperalgesia produced by peripheral injury [10–12]. Blocking gap junctions in the astrocytes suppressed hyperalgesia, which suggested that the astrocytes were processing the nociceptive information and regulating the function of spinal cord neurons . These results are similar to work reported by Hertz et al. and Ng et al. who demonstrated that astrocytes are critical for the establishment of learned behaviors [13, 14]. Furthermore, recent studies indicate that several general anesthetics suppress the function of astrocyte gap junctions at concentrations that are relevant for loss of consciousness [15, 16]. These data suggest that the anesthetic properties of these agents may be mediated at least in part by their actions on astrocytes and may indicate some role for astrocytes in consciousness.
In a recent review Robertson outlined an astrocentric hypothesis of memory  as an alternative to the current neurocentric or synaptic based theories. In this hypothesis Robertson concludes that because astrocytes form large syncytium via gap junctions and that they are connected to neurons through synapses these cells can store and "bind" diverse information. In this intriguing review Robertson hypothesizes that information is stored as a result of gap junctional plaques converting to a crystalline configuration that is a closed, high resistance, state of the gap junctions. As a result of these altered gap junctions ion flow between astrocytes is restricted resulting in a functional memory.
In examining the idea that astrocytes might play a major role in information processing it seemed prudent to examine other potential memory mechanisms that could support information processing in astrocytes. In experiments examining electrical potentials and calcium fluxes in astrocytes it was demonstrated that these cells can, on an individual basis, support potentials for several seconds [1, 2, 6, 7]. These data suggest that ion channel activity in a group of gap junction linked astrocytes could retain information for substantial periods of time. Thus, the ion channels mediating the astrocyte potentials could function to store and process information in the central nervous system. This paper examines the possible role of ion channels in storing information in astrocytes.
Results and discussion
Similarity of ion channels to cellular automata
Memory in cellular automata
In addition to examining the length of memory in cellular automata relative to the chaotic nature of the automata, Langton  evaluated how the number of units in an automaton influenced memory. In these experiments Langton used rules that produced automata that operated in the order/chaos phase transition and then varied the number of units in the automata. He found that there was a log-linear relationship between the time that the cellular automata stored information and the number of units in the automata. This indicated that the addition of units to the automata exponentially increased the amount of time the automata stored information. This relationship is an extremely powerful property of cellular automata that has evolutionary significance for biological systems that process information with ion channels. The exponential relationship between memory and the number of units in an automaton indicates that a biological system simply has to add more units (ion channels) to its calculating device in order to dramatically increase its memory. With an increase in memory duration the complexity of the calculations that can be performed also increases .
The human cellular automaton
To generate an estimate of the total number of ion channels in a human astrocyte cellular automata the number of astrocytes was approximated to be 1013 . With 106 ion channels/cell this suggests 1019 ion channels in a human cellular automaton. Using the estimate of 1019 ion channels in the human cellular automaton the predicted duration of memory was extrapolated from the slope of the line in figure 3. The relationship between memory and the number of ion channels was estimated to be . Where t is time and N is the number of ion channels in the system. This calculation yielded a predicted maximum memory for a human sized astrocyte cellular automaton of years. Therefore, for all practical purposes, the predicted maximum duration of memory in human cellular automata is infinite. What is most notable about this memory is that it occurs without fixing the information to any physical structure such as a synapse or cell as predicted in Hebb's postulate . The information is stored as a succession of representations, or ion channel configurations, with each individual representation lasting only a short period of time. The configuration of the ion channels is organized by the incoming information and then as this organization dissipates over time the information is lost. In thermodynamic terms the entropy of the system is decreased by the storage of information and, as the calculation presented above indicates, it takes a substantial amount of time for the entropy to return to baseline levels. Admittedly, the estimates for the number of ion channels and the number of astrocytes that make up a single syncytium are crude; however, even if the estimates are off by several orders of magnitude the overall conclusion that the potential duration of memory in a human ion channel cellular automaton is infinite, from a biological frame of reference, remains valid.
Associative memory in cellular automata
Another interesting facet of ion channel cellular automata is that because they are dynamic systems they can readily store temporal differences between events. In the right hand column the two events are separated by ten units of time resulting in a series of representations that differs from either the single event in the left hand column or the two simultaneous events in the middle column. These observations suggest that the proposed astrocyte memory system can associate memories and that temporal information can be stored.
Research supporting astrocyte cellular automata as memory systems
In studies published over forty years ago Hyden demonstrated that glia were critical for memory [30–32]. More recent work using the one-trial aversive learning paradigm in chicks has confirmed Hyden's findings [13, 14, 33]. In these studies inhibitors of astrocyte function were found to block both short term and intermediate term memory, but, when administered later, had no effect on the long term retention of the learned behavior. During the short and intermediate periods it was demonstrated that ion fluxes in astrocytes are critical [13, 33, 34] for memory suggesting that the astrocyte ion channels may store information in the chicks for a brief period of time, approximately 60 minutes, while the appropriate rewiring of the neuronal circuitry takes place. It is important to note that this behavioral model involves both memory and learning, while the cellular automata hypothesis presented here is related purely to memory. Memory is the ability of an organism to store information about events in a retrievable format, whereas learning involves a change in behavior or potential behavior. Thus, a consolidated learned behavior, as occurs in the one-trial aversive learning paradigm, is likely to be the result of neuronal rewiring. Furthermore, it does not require the organism to retain any specific memory of the event that precipitated the change in behavior beyond the length of time necessary to produce the rewiring. In this light, the chick in the aversive learning paradigm may actually recall the aversive stimulus for the short and intermediate term memory periods, which require astrocytes, but may not retain any recollection of the event once the aversive behavior has been established. It is enough for the chick to avoid certain objects without remembering why it needs to avoid them. The distinction between memory and learning is important because the two processes are likely mediated by different mechanisms. In the current hypothesis the ion channel cellular automata would be responsible for the specific memory of the event while changes in synaptic strength of the neurons would be responsible for learning and maintaining the new behavior. Astrocyte memory could support learning, but learning does not necessarily support the memory of events.
In addition to proposing that glia were involved in memory, Hyden predicted that mental diseases may involve glia  as reported in ). In the ion channel cellular automata hypothesis it is critical that the ion channels operate at the junction between order and chaos. Departure from this behavior is predicted to produce pathology. Deviation to the ordered side of the spectrum might produce depressive types of behaviors in the organism and memory deficits while deviation to the chaotic side might produce psychotic or manic types of behaviors that are also associated with memory deficits. Several studies have demonstrated that long term treatment with antidepressant drugs at clinically relevant doses alters protein expression and function in astrocytes [36–41] and long term treatment with lithium ion results in suppression of mRNA for sodium-dependent inositol transporter in astrocytes . The length of treatment required for the change in astrocyte proteins is consistent with the onset of the therapeutic effect of these agents. These studies suggest that these psychoactive agents may adjust the activity of astrocyte ion channel cellular automata toward the order/chaos border, thus improving the function of the memory system. Therefore, a number of studies, spanning over forty years, indicate that astrocytes are important for memory and possibly for the therapeutic effect of psychoactive drugs, which is consistent with the astrocyte ion channel cellular automata hypothesis.
In this study the hypothesis that astrocytes could store information in the central nervous system was considered. Based on the similarity of membrane ion channels to mathematical models known as cellular automata it seems reasonable to conclude that ion channels in astrocytes could store information for significant periods of time. This storage system does not rely on physically fixing information to any structure such as a synapse; rather information is stored by organizing the activity of the ion channels. If this concept is correct it suggests that neurons may use astrocytes as a dynamic information sink. In theory, this information would remain readily available to the neurons for extended periods of time. Furthermore, this hypothesis indicates that to store information for significant periods of time the ion channels in the astrocyte syncytium must be in electrical contact with each other. This function could be served by the astrocytes' gap junctions. Thus, we can predict that agents that selectively block astrocyte gap junctions should disrupt memory. Clearly, further work is needed to verify this theoretical framework for memory in nervous systems.
One dimensional cellular automaton
A 16 unit one dimensional cellular automaton was set up with each unit having 2 states. The rule used for this automaton was Wolfram's rule number 232 [20, 21]. In this rule each unit is updated by averaging the states of the unit with its two nearest neighbors and then rounding to the nearest integer. The time series for this cellular automaton was calculated by hand.
Two dimensional cellular automata
To examine the effects of different rule sets on 2 dimensional cellular automata the program CaSim  was used. A matrix of 100 × 100 units with a Moore neighborhood (eight neighbors) was set up with various rules. Each unit had 4 states. The entropy of the different rule sets was calculated using the equation entropy = -∑ Ps ln (Ps), where Ps is the probability of a unit occupying a particular state. The probabilities of the different states were determined from 10 runs of 1000 iterations for each cellular automaton. For these calculations the cellular automaton was seeded for each run by randomly setting ten percent of the units to the open state. The maximum entropy was calculated using the probability of 0.25 for each of the four states. The ratio of the calculated entropy of the rule set to the maximum possible entropy was used as an indicator of the chaotic nature of the system. Thus an entropy ratio of 0 is a completely ordered rule set and a ratio of 1 is a completely chaotic rule set.
For the examples presented in the figures the cellular automata where seeded with either 1 or 2 units set to the open state.
Duration of memory versus the number of ion channels
To calculate the relationship between the number of ion channels in a system and the duration of information storage by the ion channels data was collected from published sources. The maximum open and closed times for various ion channels were obtained [43–54] and the open to closed cycle was used as the duration of memory in single ion channels. Similarly, potentials recorded in single cells were obtained [55–62] and used as an indication of the activity of multiple ion channels in concert. The log of the values for the duration of the responses in the ion channels and cells were plotted versus the number of ion channels. The number of ion channels in the cells was estimated to be 106. A line was then fitted to the two points and the log of the duration of potentials in slices and ganglia [63–71] were plotted on the line.
This work was supported by the University of Florida College of Dentistry and the McKnight Brain Institute.
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