Grandmother Cells Are Also Widely Used in the Brain

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provided by Frontiers - Publisher Connector OPINION ARTICLE published: 24 May 2013 doi: 10.3389/fpsyg.2013.00300 An extension of the localist representation theory: grandmother cells are alsowidelyusedinthebrain

Asim Roy*

Department of Information Systems, Arizona State University, Tempe, AZ, USA *Correspondence: [email protected] Edited by: Dietmar Heinke, University of Birmingham, UK Reviewed by: Dietmar Heinke, University of Birmingham, UK

ON GRANDMOTHER CELLS multimodal, but the term came to be used fundamentally about abstraction and gen- Based on considerable neurophysiological mostly for representing a visual percept.” eralization. We, therefore, need to find evidence, Roy (2012) proposed the the- • Barlow (2009, p. 309): “The term grand- evidence for the brain’s ability to gener- ory that localist representation is widely mother cell started as a fanciful name alize and encode an abstract idea in a used in the brain, starting from the low- for a high-level neuron that might enable single cell in an invariant way. For object- est levels of processing. Grandmother cells us to experience complex perceptions related concepts, there is now plenty are a special case of localist representa- and discriminate among them. The con- of evidence for multimodal invariant tion. In this article, I present the theory cept included invariance of response for abstract cells that encode such concepts that grandmother cells are also widely used changes in some variables as well as selec- (such as the concepts of Oprah Winfrey, in the brain. To support the proposed tivity of response for others, together with Saddam Hussein, and Sydney Opera)and theory, I present neurophysiological evi- the idea that these cells are created by theevidenceispresentedinsectionThe dence and an analysis of the concept of processing at a hierarchy of levels.” Evidence for Modality Invariant Object- grandmother cells. Konorski (1967) first • Bowers (2009, p. 223): “In sum, the key related Concept Cells. There is also plenty predicted the existence of grandmother claim of localist coding schemes is that a of evidence for category-related concept cells (he called them “gnostic” neurons)— given unit (neuron) codes for one familiar cells, although they are primarily for visual single neurons that respond to complex thing (and does not directly contribute to stimuli. But, in any modality, category stimuli such as faces, hands, expressions, the representation of anything else), and cells represent an abstraction about a set objects, and so on. The term “grand- that it is possible to interpret the output of objects or features and reflect brain’s mother cell” was introduced by Jerry of a single unit in a neural network.” ability to generalize, which is the essen- Lettvin in 1969 (Barlow, 1995). tial feature of grandmother cells. And these The notion of grandmother cells is very By localist representation, Bowers implies category cells are invariant to shape, size, controversial in neuro and cognitive sci- grandmother cells. and other features of the objects in that ences. Barlow (2009, p. 320) claims that category. Thus, finding a category cell grandmother cells exist and “can now THE GRANDMOTHER CELL REPRESENTS A in any modality can be counted as evi- be recorded from and studied reliably.” COMPLEX, ABSTRACT CONCEPT dence for grandmother cells. Section The Bowers (2009) has also claimed that the For this article, let’s start with the stricter Evidence for Category Cells presents evi- brain uses grandmother cells to code for definition that a grandmother cell repre- dence for category cells in the brain. objects and concepts. However, Plaut and sents a specific and complex concept, not In the context of localist theory (Roy, McClelland (2010) and Quian Quiroga merely a percept, in a multimodal invari- 2012), grandmother cells are a special type et al. (2008; Quian Quiroga and Kreiman, ant way. Thus, the basic grandmother cell of localist cells. Roy (2012) has already 2010) have vigorously opposed the notion notion is about encoding a complex con- shown that localist cells in the brain have of grandmother cells in the brain. ceptwithinasinglecellinaninvari- “meaning and interpretation.” Therefore, ant way. And abstract categories—such the output of a grandmother cell is also THE CONCEPT OF GRANDMOTHER CELLS as animals, cars, and houses—are, with- interpretable and there is no need to revisit Grandmother cells have been character- out question, complex concepts. Category- the interpretability issue here. ized in a variety of ways. Here I reference type concepts, therefore, are part of (or some: included in) the notion of grandmother THE EVIDENCE FOR MODALITY cells. In other words, the grandmother cell INVARIANT OBJECT-RELATED • Gross (2002, p. 512): “The term “grand- notion is not necessarily restricted to just CONCEPT CELLS mother cell” refers to a neuron that would object-related concepts (such as the con- In some experiments, reported in Quian respond only to a specific, complex, and cepts of Jennifer Aniston, Saddam Hussein, Quiroga et al. (2009) and others, they meaningful stimulus, that is, to a single and Eiffel Tower), but is inclusive of the found that single medial temporal lobe percept or even a single concept. As orig- whole range of complex concepts. In a (MTL) neurons can encode an object- inally conceived, a grandmother cell was more general sense, grandmother cells are related concept irrespective of how it is

www.frontiersin.org May2013|Volume4|Article300| 1 Roy Grandmother cells used widely

presented—visual, textual, or sound. They the words “Sydney Opera,” which is obvi- activated by the patient by simply “think- check the modality invariance properties ously different in its visual properties com- ing” about Jennifer Aniston. That indi- of a neuron by showing the subjects three pared with the image of this landmark. cates the multimodal invariance property different pictures of the particular individ- Recently, it was shown that this invariance of that Jennifer Aniston cell—multimodal ual or object that a unit responds to and crosses modalities, meaning that MTL neu- because it is triggered by both visual and their spoken and written names. In these rons may exhibit a selective and “invariant” internal stimuli. And this experiment was experiments, they found (Quian Quiroga response to a particular stimulus out of 100 widely replicated—it was performed many et al., 2009, p. 1308) “aneuroninthe images and do so independently of the sen- times on many patients. left anterior hippocampus that fired selec- sory modality (visual image, audio, or writ- tively to three pictures of the television host ten iconic representations) through which THE EVIDENCE FOR CATEGORY CELLS .... Oprah Winfrey and to her written (stimu- the stimulus was presented ” Cells that represent categories have been .... lus 56) and spoken (stimulus 73) name Quian Quiroga et al. (2008) estimate found in both humans and animals. These To a lesser degree, the neuron also fired to that 40% of MTL cells are tuned to such cells reflect brain’s ability to generalize and the actress Whoopi Goldberg. None of the explicit representation. create abstractions. The invariance prop- other responses were significant, including erty is reflected in the fact that these other text and sound presentations.” They THE EVIDENCE FOR MODALITY INVARIANT cells respond to a class of objects—objects also found a neuron in the entorhinal cor- CONCEPT CELLS BASED ON “THINKING” with varying shapes, sizes, and other fea- tex of a subject that responded (Quian ABOUT A CONCEPT tures. Fried et al. (1997) found some MTL Quiroga et al., 2009, p. 1308) “selectively In the experiment by Cerf et al. (2010), neurons that respond selectively to gen- to pictures of Saddam Hussein as well as to epilepsy patients played a game to con- der and facial expression and Kreiman the text “Saddam Hussein” and his name trol the display of two superimposed et al. (2000) found MTL neurons that pronounced by the computer .... There images through four MTL neurons. Before respond to pictures of particular cate- were no responses to other pictures, texts, or the experiment, researchers identified gories of objects, such as animals, faces, sounds.” four MTL neurons in each patient that and houses. Recordings of single-neuron Quian Quiroga (2012, p. 588) reports: responded selectively to four different activity in the monkey visual temporal “Another neuron responded to Halle images. One of the four images was cortex led to the discovery of neurons Berry—even when she was masked as randomly selected to become the target that respond selectively to certain cate- Catwoman, a character she played in image. Each trial started with a short dis- gories of stimuli such as faces or objects .... one of her movies These and many play of the target image (say of Jennifer (Logothetis and Sheinberg, 1996; Tanaka, other examples suggest that MTL neurons Aniston) followed by an overlaid hybrid 1996; Freedman and Miller, 2008). encode an abstract representation of the image of the target and one of the other IquoteFreedman and Miller (2008): concept triggered by the stimulus. This three images (a distractor image, say of “These studies have revealed that the activ- claim was tested more conclusively by pre- James Brolin). The patient was then told ityofsingleneurons,particularlythosein senting the written names of these persons to enhance the target image by focusing the prefrontal and posterior parietal cortices or objects to the subjects, and it was found his/her “thoughts” on it. (Note: Perhaps (PPCs), can encode the category member- that a large proportion of MTL neurons did internal imagery in the brain was used ship, or meaning, of visual stimuli that the indeed respond to both the pictures and the by patients when asked to “think” about monkeys had learned to group into arbitrary written names of a particular individual a target image.) The initial visibility of categories.” (or object). For example, the hippocam- both images was at 50% and the visibility Lin et al. (2007) report finding “nest pal neuron that fired selectively to pictures of an image was increased or decreased cells” in mouse hippocampus that fire of Halle Berry responded also to the letter every 100 ms based on the firing rates of selectively when the mouse observes a nest string “HALLE BERRY” (and not to other the four MTL neurons. In general, if the or a bed, regardless of the location or envi- names). Moreover, the selective responses of firing rate of one neuron was higher com- ronment. these neurons could be triggered by stim- pared to the other, the image associated Gothard et al. (2007) found single neu- uli in other sensory modalities,suchasthe with that neuron became more visible. rons in the amygdala of monkeys that name of a person pronounced by a synthe- The trial was terminated when either one responded selectively to images of mon- sized voice ....” ofthetwoimageswasfullyvisibleorafter key faces, human faces, and objects as they Suthana and Fried (2012, p. 428) report a fixed time limit. The subjects success- viewed them on a computer monitor. They similar findings: “Thus, a neuron may fully reached the target, which means the found one neuron that responded in par- respond to a picture of the Sydney Opera target image was fully visible, in 596 out ticular to threatening monkey faces. Their House and exhibit no response to 50 other of 864 trials (69.0%; 202 failures and 66 general observation is (p. 1674): “These landmarks, yet also respond to many per- timeouts). examples illustrate the remarkable selectiv- mutations and physically different represen- Note that if the target image was of ityofsomeneuronsintheamygdalafor tations of the Sydney Opera House, seen Jennifer Aniston that means that they broad categories of stimuli.” in color, in black and white, or from dif- found a neuron that responded to Jennifer Thus the evidence is substantial that ferent angles. In fact, the neuron may also Aniston images and not to others. And category cells exist in the brain and that the respond to the iconic representation, namely that same Jennifer Aniston neuron was brain can abstract and generalize.

Frontiers in Psychology | Cognitive Science May 2013 | Volume 4 | Article 300 | 2 Roy Grandmother cells used widely

CONCLUSION 4th Edn., ed Michael Gazzaniga (Cambridge, MA: Plaut, D., and McClelland, J. (2010). Locating Grandmother cells are about abstract- MIT Press), 309–320. object knowledge in the brain: comment on ing complex concepts and using sin- Barlow, H. B. (1995). “The neuron doctrine in per- Bowers’s (2009) attempt to revive the grandmother ception,” in The Cognitive Neurosciences, ed M. S. cell hypothesis. Psychol. Rev. 117, 284–290. doi: gle units to encode and represent them. Gazzaniga (Cambridge, MA: MIT Press), 415–434. 10.1037/a0017101 There is obviously an efficiency aspect to Bowers, J. (2009). On the biological plausibility of Quian Quiroga, R. (2012). Concept cells: the building this. First, they provide information in grandmother cells: implications for neural net- blocks of declarative memory functions. Nat. Rev. an abstracted, summarized, and tractable work theories in psychology and neuroscience. Neurosci. 13, 587–597. doi: 10.1038/nrn3251 Psychol. 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Integrative Activity of Received: 08 April 2013; accepted: 09 May 2013; embodiment of cognitive level informa- the Brain: An Interdisciplinary Approach. published online: 24 May 2013. tion within a set of complex concept cells Chicago, IL: University of Chicago Press. doi: Citation: Roy A (2013) An extension of the localist repre- makes cognition and thought very real 10.1126/science.160.3828.652 sentation theory: grandmother cells are also widely used and easily tractable within the brain. That Kreiman, G., Koch, C., and Fried, I. (2000). Category- in the brain. Front. Psychol. 4:300. doi: 10.3389/fpsyg. makes complex concept cells extremely specific visual responses of single neurons in the 2013.00300 human medial temporal lobe. Nat. Neurosci. 3, This article was submitted to Frontiers in Cognitive valuable and fundamental to the processes 946–953. doi: 10.1038/78868 Science, a specialty of Frontiers in Psychology. that deal with cognition and thought. Lin, L. N., Chen, G. 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