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A conceptual view of memory
Episodic memory may be based on neuronal networks that extract and integrate
information from multiple sensory inputs, creating unified conceptual representations.
Rodrigo Quian Quiroga
Someone may look quite different in a series of
photos, yet we can usually tell they are the same
person. By taking advantage of brain surgery
to treat epilepsy, Rodrigo Quian Quiroga has
been able to record from individual neurons and
shed light on how the human brain achieves this
remarkable feat of recognition. In memory, he
suggests, forgetting is every bit as important as
remembering.
His investigation of memory began in earnest
in California. “It started when I was a postdoc at
CalTech with Cristof Koch. We collaborated with
Itzhak Fried, a neurosurgeon at UCLA. I had the
incredible opportunity to make recordings from
epileptic patients. This was quite unique as you
never get to record from individual neurons in
human beings, invasively.”
Interested in visual recognition, he showed
patients pictures of people or landmarks. He
discovered that certain neurons responded very
strongly – and specifically – to particular images.
“The first neuron that I found doing this was firing
to pictures of Jennifer Aniston,” he says. “It would
fire to any picture of Jennifer Aniston. It would not
fire to other actresses, other people, other places
or animals, but it would fire to seven completely
different pictures of Jennifer Aniston.”
The ‘Jennifer Aniston cell’ drew comparisons
with the fabled ‘grandmother cell’. “This is a
Morphed faces of actresses are shedding light on neural mechanisms of conscious recognition.
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BNA Bulletin
Autumn 2014
discussion that goes back to William James in the
1890s,” Professor Quian Quiroga points out. “At the
end of a sensory perception pathway, do you have
neurons that represent specific concepts such as
a grandmother?” (It was Jerry Lettvin in the late
1960s who coined the term ‘grandmother cell’ to
describe such neurons.)
Superficially, Jennifer Aniston cells may look like
grandmother cells. “But we have to be careful,” says
Professor Quian Quiroga. “If you take the extreme
definition that you have only one neuron encoding
for Jennifer Aniston and nothing else, this is clearly
not the case.” It would be a remarkable fluke to
have hit upon such a unique neuron among the
billions that could have been sampled.
It is also impossible to be sure that a neuron
has only a single real-world trigger. “In some cases
we do find neurons that fire to one concept, but we
cannot guarantee that they do not fire to anything
else because we cannot show every possible
concept in an experiment.”
Furthermore, some neurons show a degree of
promiscuity in their responses: “The neuron that
fired to Jennifer Aniston, I tested the next day
and it also fired to Lisa Kudrow, who co-starred in
the TV series Friends. A neuron that fired to Luke
Skywalker also fired to Yoda, from Star Wars. So we
do find quite often that neurons fire to more than
one concept.”
The key point, he adds, is that there are shared
features between the images that trigger firing in
individual neurons: “That’s not coincidence. That’s
exactly why we believe these neurons are involved
in encoding memories, because they are involved in
encoding links between concepts.”
Borges and Memory, Rodrigo
Quian Quiroga’s account of the
author and his ideas on memory.
“...to think is
to generalise,
to make
abstractions,
to build up
concepts.”
Conceptualisation
Indeed, as well as photographs, cells also responded
to other representations, such as written or spoken
names. “That was important, at it’s showing that
it’s not just the visual features that are triggering
the firing of the neuron. It’s the concept itself.”
His cells of interest were in the medial temporal
lobe, close to the hippocampus – areas with wellestablished roles in memory. “Then I tried to
put all this story together. The question is, why
would we have this conceptual representation
in the hippocampus? My answer is because the
basic mechanism of memory is to make links
between concepts.”
www.bna.org.uk
His idea is that Jennifer Aniston cells integrate
sensory information and, once it is clear that the
stimuli represent Jennifer Aniston (corresponding to
the subjective sense of recognition), messages are
sent to the hippocampus to retrieve the appropriate
stored information or memories.
Further work has shed light on the neural
mechanisms of this recognition. Notably, by
showing visual stimuli for very short periods,
such that participants can sometimes identify
individuals but sometimes cannot, he has been able
to uncouple visual stimulation and recognition –
revealing responses specifically associated with the
subjective experience of recognition.
Recently, he has confirmed this finding using
morphed images of, for example, Jennifer Aniston
and Jennifer Lopez. Images are adjusted until they are
recognised about half the time as Jennifer Aniston
and half as Jennifer Lopez. Although the visual input
is identical, Jennifer Aniston neurons fire only when
subjects perceive Jennifer Aniston and Jennifer Lopez
neurons only fire when the subject recognises Jennifer
Lopez. “It’s another way of showing that the neuron
follows the conscious perception of the subject rather
than the visual input.”
Notably, the timing of firing of these neurons
in the hippocampus – at about 300 ms after visual
stimuli – is significantly slower than would be
expected given the number of synapses that signals
have to travel from earlier sensory areas. This
delay, he believes, is to allow time for integration
of signals from multiple sensory systems. Analysis
of local field potentials revealed a distinctive
theta band response (at 4–8 Hz) associated
with signalling a time to fire to the hippocampal
neurons: “You can see the local field response as
an avalanche, as a massive firing of neurons that
open a time window.” A higher frequency, highgamma response, he suggests, reflects activation
of a network encoding a particular concept. Notably,
both are seen only after image recognition.
With epilepsy specialist Mark Richardson at
King’s College London, Professor Quian Quiroga
can now carry out similar studies in the UK. He
has also used EEG to explore similar questions
non-invasively, identifying specific responses
associated with face recognition – indeed, he can
decode recordings and make better-than-chance
predictions about whether a subject has recognised
a face.
This idea led him in a new direction: “After
discovering the Jennifer Aniston neurons I was
wondering what would happen if we didn’t have
these neurons. Why do we need them? Then I
remembered a short story that Borges wrote in the
1940s, ‘Funes the Memorious’, about a guy who
could remember absolutely everything.”
Rereading the story, he was startled by Borges’s
insight: “Borges argued, and I think it was brilliant
of him, that if you remember everything you
cannot even think, because to think is to generalise,
to make abstractions, to build up concepts.”
Paradoxically, to remember, we need to forget
details. “If you don’t leave details aside, you cannot
conceptualise something.”
He was struck by the fact that Borges was
describing precisely what would happen if the type
of neuron he had discovered did not exist. “So then
I started to wonder where did Borges get this idea?
I met his widow, we had many discussions about
Borges and what he knew about brain function and
so on.”
He went on to write a book, Borges and Memory,
exploring Funes, the origins of Borges’s thinking
and modern ideas about the nature of memory.
He hopes to return to the subject, to explore in
more detail how classical philosophers viewed
memory and perception, ideas that modern
neuroscience is now addressing with very different
experimental tools – including, of course, pictures
of Jennifer Aniston…
Quian Quiroga RQ et al. Invariant visual representation by single neurons
in the human brain. Nature. 2005;435(7045):1102–7.
Quian Quiroga RQ et al. Human single-neuron responses at the threshold
of conscious recognition. Proc Natl Acad Sci USA. 2008;105(9):3599–604.
Quian Quiroga R, Kraskov A, Koch C, Fried I. Explicit encoding of
multimodal percepts by single neurons in the human brain. Curr Biol.
2009;19(15):1308–13.
Rey HG, Fried I, Quian Quiroga R. Timing of single-neuron and local
field potential responses in the human medial temporal lobe. Curr Biol.
2014;24(3):299–304
Navajas J, Ahmadi M, Quian Quiroga R. Uncovering the mechanisms of
conscious face perception: a single-trial study of the n170 responses.
J Neurosci. 2013;33(4):1337–43.
Quian Quiroga R et al. Single-Cell Responses to Face Adaptation in the
Human Medial Temporal Lobe. Neuron 2014;84:1–7.
Rodrigo Quian Quiroga: www2.le.ac.uk/centres/csn/people-1/Rodrigo
Centre for Systems Neuroscience: www2.le.ac.uk/centres/csn
Making memories
The findings, he argues, point to the idea of
memory as abstraction, or extraction of meaning.
The brain does not capture a film of life that
can be rewound and replayed, but draws out key
conceptual elements that can be linked together.
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Autumn 2014 BNA Bulletin
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